Stem cells and targeted approaches to melanoma cure

Molecular Aspects of Medicine

Volumn 39, Issue , 2014, Pages 33-49

  Murphy, George F ^a   Wilson, Brian J ^a,b   Girouard, Sasha D ^c   Frank, Natasha Y ^d   Frank, Markus H ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

ABCB5; Cancer stem cell; Drug resistance; Immune evasion; Melanoma; Therapy; Vasculogenic mimicry

Indexed keywords

ABC TRANSPORTER B5; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; CD133 ANTIGEN; CD134 ANTIGEN; CD86 ANTIGEN; DACARBAZINE; GLYCOPROTEIN 100 PEPTIDE VACCINE; INTERLEUKIN 10; INTERLEUKIN 2; IPILIMUMAB; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OX40 LIGAND; PEPTIDE VACCINE; PROGRAMMED DEATH 1 RECEPTOR; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TEMOZOLOMIDE; THALIDOMIDE; TICILIMUMAB; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VEMURAFENIB;

ADAPTIVE IMMUNITY; CANCER GROWTH; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL RENEWAL; CELL SUBPOPULATION; CHEMOSENSITIZATION; CIRCULATING TUMOR CELL; CLINICAL EFFECTIVENESS; CYTOKINE PRODUCTION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; IMMUNOCOMPETENCE; IMMUNOLOGICAL TOLERANCE; LUNG METASTASIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA; MELANOMA CELL; MELANOMA STEM CELL; METASTATIC MELANOMA; MOLECULARLY TARGETED THERAPY; NONHUMAN; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; TUMOR IMMUNITY; ANIMAL; DRUG RESISTANCE; IMMUNOLOGY; METABOLISM; PATHOLOGY; TRANSPLANTATION;

ANIMALS; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MELANOMA; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS;

EID: 84906959992     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2013.10.003     Document Type: Review

References (131)

1. C. Aleman, J.P. Annereau, X.J. Liang, C.O. Cardarelli, B. Taylor, J.J. Yin, A. Aszalos, and M.M. Gottesman P-glycoprotein, expressed in multidrug resistant cells, is not responsible for alterations in membrane fluidity or membrane potential Cancer Res. 63 12 2003 3084 3091
2. R. Allikmets, L.M. Schriml, A. Hutchinson, V. Romano-Spica, and M. Dean A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance Cancer Res. 58 23 1998 5337 5339
3. S.R. Alonso, L. Tracey, P. Ortiz, B. Perez-Gomez, J. Palacios, M. Pollan, J. Linares, S. Serrano, A.I. Saez-Castillo, L. Sanchez, R. Pajares, A. Sanchez-Aguilera, M.J. Artiga, M.A. Piris, and J.L. Rodriguez-Peralto A high-throughput study in melanoma identifies epithelial-mesenchymal transition as a major determinant of metastasis Cancer Res. 67 7 2007 3450 3460
4. N. Aptsiauri, T. Cabrera, R. Mendez, A. Garcia-Lora, F. Ruiz-Cabello, and F. Garrido Role of altered expression of HLA class I molecules in cancer progression Adv. Exp. Med. Biol. 601 2007 123 131
5. C. Arce, C. Perez-Plasencia, A. Gonzalez-Fierro, E. de la Cruz-Hernandez, A. Revilla-Vazquez, A. Chavez-Blanco, C. Trejo-Becerril, E. Perez-Cardenas, L. Taja-Chayeb, E. Bargallo, P. Villarreal, T. Ramirez, T. Vela, M. Candelaria, M.F. Camargo, E. Robles, and A. Duenas-Gonzalez A proof-of-principle study of epigenetic therapy added to neoadjuvant doxorubicin cyclophosphamide for locally advanced breast cancer PLoS ONE 1 2006 e98
6. A.S. Azevedo, B. Grotek, A. Jacinto, G. Weidinger, and L. Saude The regenerative capacity of the zebrafish caudal fin is not affected by repeated amputations PLoS ONE 6 7 2011 e22820
7. M. Bittner, P. Meltzer, Y. Chen, Y. Jiang, E. Seftor, M. Hendrix, M. Radmacher, R. Simon, Z. Yakhini, A. Ben-Dor, N. Sampas, E. Dougherty, E. Wang, F. Marincola, C. Gooden, J. Lueders, A. Glatfelter, P. Pollock, J. Carpten, E. Gillanders, D. Leja, K. Dietrich, C. Beaudry, M. Berens, D. Alberts, and V. Sondak Molecular classification of cutaneous malignant melanoma by gene expression profiling Nature 406 6795 2000 536 540
8. A.D. Boiko, O.V. Razorenova, M. van de Rijn, S.M. Swetter, D.L. Johnson, D.P. Ly, P.D. Butler, G.P. Yang, B. Joshua, M.J. Kaplan, M.T. Longaker, and I.L. Weissman Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271 Nature 466 7302 2010 133 137
9. N. Bonitsis, A. Batistatou, S. Karantima, and K. Charalabopoulos The role of cadherin/catenin complex in malignant melanoma Exp. Oncol. 28 3 2006 187 193
10. J.B. Boonyaratanakornkit, L. Yue, L.R. Strachan, K.J. Scalapino, P.E. LeBoit, Y. Lu, S.P. Leong, J.E. Smith, and R. Ghadially Selection of tumorigenic melanoma cells using ALDH J. Invest. Dermatol. 130 12 2010 2799 2808
11. T. Cabrera, E. Lara, J.M. Romero, I. Maleno, L.M. Real, F. Ruiz-Cabello, P. Valero, F.M. Camacho, and F. Garrido HLA class I expression in metastatic melanoma correlates with tumor development during autologous vaccination Cancer Immunol. Immunother. 56 5 2007 709 717
12. L.H. Camacho, S. Antonia, J. Sosman, J.M. Kirkwood, T.F. Gajewski, B. Redman, D. Pavlov, C. Bulanhagui, V.A. Bozon, J. Gomez-Navarro, and A. Ribas Phase I/II trial of tremelimumab in patients with metastatic melanoma J. Clin. Oncol. 27 7 2009 1075 1081
13. J. Cao, L. Wan, E. Hacker, X. Dai, S. Lenna, C. Jimenez-Cervantes, Y. Wang, N.R. Leslie, G.X. Xu, H.R. Widlund, B. Ryu, R.M. Alani, K. Dutton-Regester, C.R. Goding, N.K. Hayward, W. Wei, and R. Cui MC1R is a potent regulator of PTEN after UV exposure in melanocytes Mol. Cell 51 4 2013 409 422
14. R. Carretero, J.M. Romero, F. Ruiz-Cabello, I. Maleno, F. Rodriguez, F.M. Camacho, L.M. Real, F. Garrido, and T. Cabrera Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy Immunogenetics 60 8 2008 439 447
15. M. Chartrain, J. Riond, A. Stennevin, I. Vandenberghe, B. Gomes, L. Lamant, N. Meyer, J.E. Gairin, N. Guilbaud, and J.P. Annereau Melanoma chemotherapy leads to the selection of ABCB5-expressing cells PLoS ONE 7 5 2012 e36762
16. P.M. Chaudhary, and I.B. Roninson Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells Cell 66 1 1991 85 94
17. P.F. Cheung, C.K. Cheng, N.C. Wong, J.C. Ho, C.W. Yip, V.C. Lui, A.N. Cheung, S.T. Fan, and S.T. Cheung Granulin-epithelin precursor is an oncofetal protein defining hepatic cancer stem cells PLoS ONE 6 12 2011 e28246
18. W.C. Chou, M. Takeo, P. Rabbani, H. Hu, W. Lee, Y.R. Chung, J. Carucci, P. Overbeek, and M. Ito Direct migration of follicular melanocyte stem cells to the epidermis after wounding or UVB irradiation is dependent on Mc1r signaling Nat. Med. 19 7 2013 924 929
19. G. Civenni, A. Walter, N. Kobert, D. Mihic-Probst, M. Zipser, B. Belloni, B. Seifert, H. Moch, R. Dummer, M. van den Broek, and L. Sommer Human CD271-positive melanoma stem cells associated with metastasis establish tumor heterogeneity and long-term growth Cancer Res. 71 8 2011 3098 3109
20. W.H. Clark Jr., L. From, E.A. Bernardino, and M.C. Mihm The histogenesis and biologic behavior of primary human malignant melanomas of the skin Cancer Res. 29 3 1969 705 727
21. M.F. Clarke, J.E. Dick, P.B. Dirks, C.J. Eaves, C.H. Jamieson, D.L. Jones, J. Visvader, I.L. Weissman, and G.M. Wahl Cancer stem cells-perspectives on current status and future directions: AACR workshop on cancer stem cells Cancer Res. 66 19 2006 9339 9344
22. S.P. Cole, G. Bhardwaj, J.H. Gerlach, J.E. Mackie, C.E. Grant, K.C. Almquist, A.J. Stewart, E.U. Kurz, A.M. Duncan, and R.G. Deeley Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line Science 258 5088 1992 1650 1654
23. E. Colombo, S. Romaggi, F. Blasevich, M. Mora, C. Falcone, H. Lochmuller, L. Morandi, and C. Farina The neurotrophin receptor p75NTR is induced on mature myofibres in inflammatory myopathies and promotes myotube survival to inflammatory stress Neuropathol. Appl. Neurobiol. 38 4 2012 367 378
24. L.A. Doyle, W. Yang, L.V. Abruzzo, T. Krogmann, Y. Gao, A.K. Rishi, and D.D. Ross A multidrug resistance transporter from human MCF-7 breast cancer cells Proc. Natl. Acad. Sci. USA 95 26 1998 15665 15670
25. A.M. Elliott, and M.A. Al-Hajj ABCB8 mediates doxorubicin resistance in melanoma cells by protecting the mitochondrial genome Mol. Cancer Res. 7 1 2009 79 87
26. Y.Z. Fan, and W. Sun Molecular regulation of vasculogenic mimicry in tumors and potential tumor-target therapy World J. Gastrointest. Surg. 2 4 2010 117 127
27. D. Fang, T.K. Nguyen, K. Leishear, R. Finko, A.N. Kulp, S. Hotz, P.A. Van Belle, X. Xu, D.E. Elder, and M. Herlyn A tumorigenic subpopulation with stem cell properties in melanomas Cancer Res. 65 20 2005 9328 9337
28. C. Fiorentini, N. Guerra, M. Facchetti, A. Finardi, L. Tiberio, L. Schiaffonati, P. Spano, and C. Missale Nerve growth factor regulates dopamine D(2) receptor expression in prolactinoma cell lines via p75(NGFR)-mediated activation of nuclear factor-kappaB Mol. Endocrinol. 16 2 2002 353 366
29. R. Folberg, M.J. Hendrix, and A.J. Maniotis Vasculogenic mimicry and tumor angiogenesis Am. J. Pathol. 156 2 2000 361 381
30. N.Y. Frank, S.S. Pendse, P.H. Lapchak, A. Margaryan, D. Shlain, C. Doeing, M.H. Sayegh, and M.H. Frank Regulation of progenitor cell fusion by ABCB5 P-glycoprotein, a novel human ATP-binding cassette transporter J. Biol. Chem. 278 47 2003 47156 47165
31. N.Y. Frank, A. Margaryan, Y. Huang, T. Schatton, A.M. Waaga-Gasser, M. Gasser, M.H. Sayegh, W. Sadee, and M.H. Frank ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma Cancer Res. 65 10 2005 4320 4333
32. N.Y. Frank, T. Schatton, and M.H. Frank The therapeutic promise of the cancer stem cell concept J. Clin. Invest. 120 1 2010 41 50
33. N.Y. Frank, T. Schatton, S. Kim, Q. Zhan, B.J. Wilson, J. Ma, K.R. Saab, V. Osherov, H.R. Widlund, M. Gasser, A.M. Waaga-Gasser, T.S. Kupper, G.F. Murphy, and M.H. Frank VEGFR-1 expressed by malignant melanoma-initiating cells is required for tumor growth Cancer Res. 71 4 2011 1474 1485
34. M. Fukunaga-Kalabis, G. Martinez, T.K. Nguyen, D. Kim, A. Santiago-Walker, A. Roesch, and M. Herlyn Tenascin-C promotes melanoma progression by maintaining the ABCB5-positive side population Oncogene 29 46 2010 6115 6124
35. S.D. Girouard, A.C. Laga, M.C. Mihm, R.A. Scolyer, J.F. Thompson, Q. Zhan, H.R. Widlund, C.W. Lee, and G.F. Murphy SOX2 contributes to melanoma cell invasion Lab. Invest. 92 3 2012 362 370
36. B.C. Gleason, C.P. Crum, and G.F. Murphy Expression patterns of MITF during human cutaneous embryogenesis: evidence for bulge epithelial expression and persistence of dermal melanoblasts J. Cutan. Pathol. 35 7 2008 615 622
37. M.A. Goodell, K. Brose, G. Paradis, A.S. Conner, and R.C. Mulligan Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo J. Exp. Med. 183 4 1996 1797 1806
38. M.A. Goodell, M. Rosenzweig, H. Kim, D.F. Marks, M. DeMaria, G. Paradis, S.A. Grupp, C.A. Sieff, R.C. Mulligan, and R.P. Johnson Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species Nat. Med. 3 12 1997 1337 1345
39. M.M. Gottesman, T. Fojo, and S.E. Bates Multidrug resistance in cancer: role of ATP-dependent transporters Nat. Rev. Cancer 2 1 2002 48 58
40. R.J. Greenwald, G.J. Freeman, and A.H. Sharpe The B7 family revisited Annu. Rev. Immunol. 23 2005 515 548
41. P. Gros, Y.B. Ben Neriah, J.M. Croop, and D.E. Housman Isolation and expression of a complementary DNA that confers multidrug resistance Nature 323 6090 1986 728 731
42. M.J. Hendrix, E.A. Seftor, A.R. Hess, and R.E. Seftor Molecular plasticity of human melanoma cells Oncogene 22 20 2003 3070 3075
43. M.J. Hendrix, E.A. Seftor, A.R. Hess, and R.E. Seftor Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma Nat. Rev. Cancer 3 6 2003 411 421
44. C.F. Higgins ABC transporters: from microorganisms to man Annu. Rev. Cell Biol. 8 1992 67 113
45. F.S. Hodi, S.J. O'Day, D.F. McDermott, R.W. Weber, J.A. Sosman, J.B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J.C. Hassel, W. Akerley, A.J. van den Eertwegh, J. Lutzky, P. Lorigan, J.M. Vaubel, G.P. Linette, D. Hogg, C.H. Ottensmeier, C. Lebbe, C. Peschel, I. Quirt, J.I. Clark, J.D. Wolchok, J.S. Weber, J. Tian, M.J. Yellin, G.M. Nichol, A. Hoos, and W.J. Urba Improved survival with ipilimumab in patients with metastatic melanoma N. Engl. J. Med. 363 8 2010 711 723
46. J.D. Hoerter, P. Bradley, A. Casillas, D. Chambers, B. Weiswasser, L. Clements, S. Gilbert, and A. Jiao Does melanoma begin in a melanocyte stem cell? J. Skin Cancer 2012 2012 571087
47. M.Y. Hsu, F. Meier, and M. Herlyn Melanoma development and progression: a conspiracy between tumor and host Differentiation 70 9-10 2002 522 536
48. Y. Huang, P. Anderle, K.J. Bussey, C. Barbacioru, U. Shankavaram, Z. Dai, W.C. Reinhold, A. Papp, J.N. Weinstein, and W. Sadee Membrane transporters and channels: role of the transportome in cancer chemosensitivity and chemoresistance Cancer Res. 64 12 2004 4294 4301
49. R.N. Kelsh, B. Schmid, and J.S. Eisen Genetic analysis of melanophore development in zebrafish embryos Dev. Biol. 225 2 2000 277 293
50. G.I. Keshet, I. Goldstein, O. Itzhaki, K. Cesarkas, L. Shenhav, A. Yakirevitch, A.J. Treves, J. Schachter, N. Amariglio, and G. Rechavi MDR1 expression identifies human melanoma stem cells Biochem. Biophys. Res. Commun. 368 4 2008 930 936
51. H.T. Khong, Q.J. Wang, and S.A. Rosenberg Identification of multiple antigens recognized by tumor-infiltrating lymphocytes from a single patient: tumor escape by antigen loss and loss of MHC expression J. Immunother. 27 3 2004 184 190
52. W.M. Klein, B.P. Wu, S. Zhao, H. Wu, A.J. Klein-Szanto, and S.R. Tahan Increased expression of stem cell markers in malignant melanoma Mod. Pathol. 20 1 2007 102 107
53. V. Kupas, C. Weishaupt, D. Siepmann, M.L. Kaserer, M. Eickelmann, D. Metze, T.A. Luger, S. Beissert, and K. Loser RANK is expressed in metastatic melanoma and highly upregulated on melanoma-initiating cells J. Invest. Dermatol. 131 4 2011 944 955
54. A.C. Laga, and G.F. Murphy Cellular heterogeneity in vertical growth phase melanoma Arch. Pathol. Lab. Med. 134 12 2010 1750 1757
55. A.C. Laga, C.Y. Lai, Q. Zhan, S.J. Huang, E.F. Velazquez, Q. Yang, M.Y. Hsu, and G.F. Murphy Expression of the embryonic stem cell transcription factor SOX2 in human skin: relevance to melanocyte and merkel cell biology Am. J. Pathol. 176 2 2010 903 913
56. A.C. Laga, Q. Zhan, C. Weishaupt, J. Ma, M.H. Frank, and G.F. Murphy SOX2 and nestin expression in human melanoma: an immunohistochemical and experimental study Exp. Dermatol. 20 4 2011 339 345
57. J.T. Lee, and M. Herlyn Microenvironmental influences in melanoma progression J. Cell. Biochem. 101 4 2007 862 872
58. P.P. Lee, C. Yee, P.A. Savage, L. Fong, D. Brockstedt, J.S. Weber, D. Johnson, S. Swetter, J. Thompson, P.D. Greenberg, M. Roederer, and M.M. Davis Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients Nat. Med. 5 6 1999 677 685
59. T. Leemhuis, M.C. Yoder, S. Grigsby, B. Aguero, P. Eder, and E.F. Srour Isolation of primitive human bone marrow hematopoietic progenitor cells using Hoechst 33342 and Rhodamine 123 Exp. Hematol. 24 10 1996 1215 1224
60. L. Li, M. Fukunaga-Kalabis, and M. Herlyn Isolation and cultivation of dermal stem cells that differentiate into functional epidermal melanocytes Methods Mol. Biol. 806 2012 15 29
61. C.G. Lian, Y. Xu, C. Ceol, F. Wu, A. Larson, K. Dresser, W. Xu, L. Tan, Y. Hu, Q. Zhan, C.W. Lee, D. Hu, B.Q. Lian, S. Kleffel, Y. Yang, J. Neiswender, A.J. Khorasani, R. Fang, C. Lezcano, L.M. Duncan, R.A. Scolyer, J.F. Thompson, H. Kakavand, Y. Houvras, L.I. Zon, M.C. Mihm Jr., U.B. Kaiser, T. Schatton, B.A. Woda, G.F. Murphy, and Y.G. Shi Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma Cell 150 6 2012 1135 1146
62. J.Y. Lin, and D.E. Fisher Melanocyte biology and skin pigmentation Nature 445 7130 2007 843 850
63. J.Y. Lin, M. Zhang, T. Schatton, B.J. Wilson, A. Alloo, J. Ma, A.A. Qureshi, N.Y. Frank, J. Han, and M.H. Frank Genetically determined ABCB5 functionality correlates with pigmentation phenotype and melanoma risk Biochem. Biophys. Res. Commun. 436 3 2013 536 542
64. P.C. Lunter, J.W. van Kilsdonk, H. van Beek, I.M. Cornelissen, M. Bergers, P.H. Willems, G.N. van Muijen, and G.W. Swart Activated leukocyte cell adhesion molecule (ALCAM/CD166/MEMD), a novel actor in invasive growth, controls matrix metalloproteinase activity Cancer Res. 65 19 2005 8801 8808
65. Y. Luo, K. Dallaglio, Y. Chen, W.A. Robinson, S.E. Robinson, M.D. McCarter, J. Wang, R. Gonzalez, D.C. Thompson, D.A. Norris, D.R. Roop, V. Vasiliou, and M. Fujita ALDH1A isozymes are markers of human melanoma stem cells and potential therapeutic targets Stem Cells 30 10 2012 2100 2113
66. J. Ma, J.Y. Lin, A. Alloo, B.J. Wilson, T. Schatton, Q. Zhan, G.F. Murphy, A.M. Waaga-Gasser, M. Gasser, F. Stephen Hodi, N.Y. Frank, and M.H. Frank Isolation of tumorigenic circulating melanoma cells Biochem. Biophys. Res. Commun. 402 4 2012 711 717
67. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, M. Shipitsin, L.L. Campbell, K. Polyak, C. Brisken, J. Yang, and R.A. Weinberg The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 4 2008 704 715
68. A.J. Maniotis, R. Folberg, A. Hess, E.A. Seftor, L.M. Gardner, J. Pe'er, J.M. Trent, P.S. Meltzer, and M.J. Hendrix Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry Am. J. Pathol. 155 3 1999 739 752
69. J.C. McAllister, Q. Zhan, C. Weishaupt, M.Y. Hsu, and G.F. Murphy The embryonic morphogen, nodal, is associated with channel-like structures in human malignant melanoma xenografts J. Cutan. Pathol. 37 Suppl 1 2010 19 25
70. E. Monzani, F. Facchetti, E. Galmozzi, E. Corsini, A. Benetti, C. Cavazzin, A. Gritti, A. Piccinini, D. Porro, M. Santinami, G. Invernici, E. Parati, G. Alessandri, and C.A. La Porta Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential Eur. J. Cancer 43 5 2007 935 946
71. A.P. Morel, M. Lievre, C. Thomas, G. Hinkal, S. Ansieau, and A. Puisieux Generation of breast cancer stem cells through epithelial-mesenchymal transition PLoS ONE 3 8 2008 e2888
72. Y.R. Na, S.H. Seok, D.J. Kim, J.H. Han, T.H. Kim, H. Jung, B.H. Lee, and J.H. Park Bone morphogenetic protein 7 induces mesenchymal-to-epithelial transition in melanoma cells, leading to inhibition of metastasis Cancer Sci. 100 11 2009 2218 2225
73. E.K. Nishimura Melanocyte stem cells: a melanocyte reservoir in hair follicles for hair and skin pigmentation Pigment Cell Melanoma Res. 24 3 2011 401 410
74. E.K. Nishimura, S.R. Granter, and D.E. Fisher Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche Science 307 5710 2005 720 724
75. C.A. O'Brien, A. Pollett, S. Gallinger, and J.E. Dick A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature 445 7123 2007 106 110
76. T. O'Reilly-Pol, and S.L. Johnson Neocuproine ablates melanocytes in adult zebrafish Zebrafish 5 4 2008 257 264
77. T. O'Reilly-Pol, and S.L. Johnson Melanocyte regeneration reveals mechanisms of adult stem cell regulation Semin. Cell Dev. Biol. 20 1 2009 117 124
78. S.G. Piccirillo, B.A. Reynolds, N. Zanetti, G. Lamorte, E. Binda, G. Broggi, H. Brem, A. Olivi, F. Dimeco, and A.L. Vescovi Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells Nature 444 7120 2006 761 765
79. G.B. Pierce The cancer cell and its control by the embryo. Rous-Whipple Award lecture Am. J. Pathol. 113 1 1983 117 124
80. E. Quintana, M. Shackleton, M.S. Sabel, D.R. Fullen, T.M. Johnson, and S.J. Morrison Efficient tumour formation by single human melanoma cells Nature 456 7222 2008 593 598
81. E. Quintana, M. Shackleton, H.R. Foster, D.R. Fullen, M.S. Sabel, T.M. Johnson, and S.J. Morrison Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized Cancer Cell 18 5 2010 510 523
82. G. Rappa, O. Fodstad, and A. Lorico The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma Stem Cells 26 12 2008 3008 3017
83. A.L. Reid, M. Millward, R. Pearce, M. Lee, M.H. Frank, A. Ireland, L. Monshizadeh, T. Rai, P. Heenan, S. Medic, P. Kumarasinghe, and M. Ziman Markers of circulating tumour cells in the peripheral blood of patients with melanoma correlate with disease recurrence and progression Br. J. Dermatol. 168 1 2013 85 92
84. A. Ribas, L.H. Camacho, G. Lopez-Berestein, D. Pavlov, C.A. Bulanhagui, R. Millham, B. Comin-Anduix, J.M. Reuben, E. Seja, C.A. Parker, A. Sharma, J.A. Glaspy, and J. Gomez-Navarro Antitumor activity in melanoma and anti-self responses in a phase I trial with the anti-cytotoxic T lymphocyte-associated antigen 4 monoclonal antibody CP-675,206 J. Clin. Oncol. 23 35 2005 8968 8977
85. L. Ricci-Vitiani, D.G. Lombardi, E. Pilozzi, M. Biffoni, M. Todaro, C. Peschle, and R. De Maria Identification and expansion of human colon-cancer-initiating cells Nature 445 7123 2007 111 115
86. J.R. Riordan, K. Deuchars, N. Kartner, N. Alon, J. Trent, and V. Ling Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines Nature 316 6031 1985 817 819
87. A. Roesch, M. Fukunaga-Kalabis, E.C. Schmidt, S.E. Zabierowski, P.A. Brafford, A. Vultur, D. Basu, P. Gimotty, T. Vogt, and M. Herlyn A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth Cell 141 4 2010 583 594
88. M.G. Roncarolo, S. Gregori, M. Battaglia, R. Bacchetta, K. Fleischhauer, and M.K. Levings Interleukin-10-secreting type 1 regulatory T cells in rodents and humans Immunol. Rev. 212 2006 28 50
89. I.B. Roninson, J.E. Chin, K.G. Choi, P. Gros, D.E. Housman, A. Fojo, D.W. Shen, M.M. Gottesman, and I. Pastan Isolation of human mdr DNA sequences amplified in multidrug-resistant KB carcinoma cells Proc. Natl. Acad. Sci. USA 83 12 1986 4538 4542
90. S.A. Rosenberg, J.C. Yang, and N.P. Restifo Cancer immunotherapy: moving beyond current vaccines Nat. Med. 10 9 2004 909 915
91. T. Rothhammer, F. Bataille, T. Spruss, G. Eissner, and A.K. Bosserhoff Functional implication of BMP4 expression on angiogenesis in malignant melanoma Oncogene 26 28 2007 4158 4170
92. D.M. Rothstein, and M.H. Sayegh T-cell costimulatory pathways in allograft rejection and tolerance Immunol. Rev. 196 2003 85 108
93. T. Schatton, and M.H. Frank Antitumor immunity and cancer stem cells Ann. N. Y. Acad. Sci. 1176 2009 154 169
94. T. Schatton, G.F. Murphy, N.Y. Frank, K. Yamaura, A.M. Waaga-Gasser, M. Gasser, Q. Zhan, S. Jordan, L.M. Duncan, C. Weishaupt, R.C. Fuhlbrigge, T.S. Kupper, M.H. Sayegh, and M.H. Frank Identification of cells initiating human melanomas Nature 451 7176 2008 345 349
95. T. Schatton, U. Schutte, N.Y. Frank, Q. Zhan, A. Hoerning, S.C. Robles, J. Zhou, F.S. Hodi, G.C. Spagnoli, G.F. Murphy, and M.H. Frank Modulation of T-cell activation by malignant melanoma initiating cells Cancer Res. 70 2 2010 697 708
96. M. Schlaak, P. Schmidt, C. Bangard, P. Kurschat, C. Mauch, and H. Abken Regression of metastatic melanoma in a patient by antibody targeting of cancer stem cells Oncotarget 3 1 2012 22 30
97. P. Schmidt, C. Kopecky, A. Hombach, P. Zigrino, C. Mauch, and H. Abken Eradication of melanomas by targeted elimination of a minor subset of tumor cells Proc. Natl. Acad. Sci. USA 108 6 2011 2474 2479
98. R.E. Seftor, E.A. Seftor, N. Koshikawa, P.S. Meltzer, L.M. Gardner, M. Bilban, W.G. Stetler-Stevenson, V. Quaranta, and M.J. 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. 61 17 2001 6322 6327
99. E.A. Seftor, P.S. Meltzer, G.C. Schatteman, L.M. Gruman, A.R. Hess, D.A. Kirschmann, R.E. Seftor, and M.J. Hendrix Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: role in vasculogenic mimicry Crit. Rev. Oncol. Hematol. 44 1 2002 17 27
100. O. Shakhova, and L. Sommer Testing the cancer stem cell hypothesis in melanoma: the clinics will tell Cancer Lett. 338 1 2013 74 81
101. B.K. Sharma, V. Manglik, and E.G. Elias Immuno-expression of human melanoma stem cell markers in tissues at different stages of the disease J. Surg. Res. 163 1 2010 e11 e15
102. S.K. Singh, C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, T. Hide, R.M. Henkelman, M.D. Cusimano, and P.B. Dirks Identification of human brain tumour initiating cells Nature 432 7015 2004 396 401
103. G.J. Spangrude, and G.R. Johnson Resting and activated subsets of mouse multipotent hematopoietic stem cells Proc. Natl. Acad. Sci. USA 87 19 1990 7433 7437
104. G.J. Spangrude, D.M. Brooks, and D.B. Tumas Long-term repopulation of irradiated mice with limiting numbers of purified hematopoietic stem cells: in vivo expansion of stem cell phenotype but not function Blood 85 4 1995 1006 1016
105. J.L. Spees, S.D. Olson, J. Ylostalo, P.J. Lynch, J. Smith, A. Perry, A. Peister, M.Y. Wang, and D.J. Prockop Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma Proc. Natl. Acad. Sci. USA 100 5 2003 2397 2402
106. E. Stockert, E. Jager, Y.T. Chen, M.J. Scanlan, I. Gout, J. Karbach, M. Arand, A. Knuth, and L.J. Old A survey of the humoral immune response of cancer patients to a panel of human tumor antigens J. Exp. Med. 187 8 1998 1349 1354
107. N. Terada, T. Hamazaki, M. Oka, M. Hoki, D.M. Mastalerz, Y. Nakano, E.M. Meyer, L. Morel, B.E. Petersen, and E.W. Scott Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion Nature 416 6880 2002 542 545
108. J.P. Thiery Epithelial-mesenchymal transitions in tumour progression Nat. Rev. Cancer 2 6 2002 442 454
109. A. Thies, U. Mangold, I. Moll, and U. Schumacher PAS-positive loops and networks as a prognostic indicator in cutaneous malignant melanoma J. Pathol. 195 5 2001 537 542
110. J.M. Topczewska, L.M. Postovit, N.V. Margaryan, A. Sam, A.R. Hess, W.W. Wheaton, B.J. Nickoloff, J. Topczewski, and M.J. Hendrix Embryonic and tumorigenic pathways converge via nodal signaling: role in melanoma aggressiveness Nat. Med. 12 8 2006 925 932
111. C. Turner, and M. Kohandel Investigating the link between epithelial-mesenchymal transition and the cancer stem cell phenotype: a mathematical approach J. Theor. Biol. 265 3 2010 329 335
112. K. Ueda, M.M. Cornwell, M.M. Gottesman, I. Pastan, I.B. Roninson, V. Ling, and J.R. Riordan The mdr1 gene, responsible for multidrug-resistance, codes for P-glycoprotein Biochem. Biophys. Res. Commun. 141 3 1986 956 962
113. A.M. Van der Bliek, F. Baas, Ten Houte, T. de Lange, P.M. Kooiman, T. Van der Velde-Koerts, and P. Borst The human mdr3 gene encodes a novel P-glycoprotein homologue and gives rise to alternatively spliced mRNAs in liver EMBO J. 6 11 1987 3325 3331
114. D.W. van der Schaft, R.E. Seftor, E.A. Seftor, A.R. Hess, L.M. Gruman, D.A. Kirschmann, Y. Yokoyama, A.W. Griffioen, and M.J. Hendrix Effects of angiogenesis inhibitors on vascular network formation by human endothelial and melanoma cells J. Natl. Cancer Inst. 96 19 2004 1473 1477
115. I.S. van Houdt, B.J. Sluijter, L.M. Moesbergen, W.M. Vos, T.D. de Gruijl, B.G. Molenkamp, A.J. van den Eertwegh, E. Hooijberg, P.A. van Leeuwen, C.J. Meijer, and J.J. Oudejans Favorable outcome in clinically stage II melanoma patients is associated with the presence of activated tumor infiltrating T-lymphocytes and preserved MHC class I antigen expression Int. J. Cancer 123 3 2008 609 615
116. L.C. van Kempen, F. Meier, M. Egeblad, M.J. Kersten-Niessen, C. Garbe, U.H. Weidle, G.N. Van Muijen, M. Herlyn, H.P. Bloemers, and G.W. Swart Truncation of activated leukocyte cell adhesion molecule: a gateway to melanoma metastasis J. Invest. Dermatol. 122 5 2004 1293 1301
117. I. Vasquez-Moctezuma, M.A. Meraz-Rios, C.G. Villanueva-Lopez, M. Magana, R. Martinez-Macias, D.J. Sanchez-Gonzalez, F. Garcia-Sierra, and N.E. Herrera-Gonzalez ATP-binding cassette transporter ABCB5 gene is expressed with variability in malignant melanoma Actas Dermosifiliogr 101 4 2010 341 348
118. G. Vassilopoulos, P.R. Wang, and D.W. Russell Transplanted bone marrow regenerates liver by cell fusion Nature 422 6934 2003 901 904
119. X. Wang, H. Willenbring, Y. Akkari, Y. Torimaru, M. Foster, M. Al-Dhalimy, E. Lagasse, M. Finegold, S. Olson, and M. Grompe Cell fusion is the principal source of bone-marrow-derived hepatocytes Nature 422 6934 2003 897 901
120. M.A. Warso, A.J. Maniotis, X. Chen, D. Majumdar, M.K. Patel, A. Shilkaitis, T.K. Gupta, and R. Folberg Prognostic significance of periodic acid-Schiff-positive patterns in primary cutaneous melanoma Clin. Cancer Res. 7 3 2001 473 477
121. J. Weber, J.A. Thompson, O. Hamid, D. Minor, A. Amin, I. Ron, R. Ridolfi, H. Assi, A. Maraveyas, D. Berman, J. Siegel, and S.J. O'Day A randomized, double-blind, placebo-controlled, phase II study comparing the tolerability and efficacy of ipilimumab administered with or without prophylactic budesonide in patients with unresectable stage III or IV melanoma Clin. Cancer Res. 15 17 2009 5591 5598
122. B.J. Wilson, T. Schatton, Q. Zhan, M. Gasser, J. Ma, K.R. Saab, R. Schanche, A.M. Waaga-Gasser, J.S. Gold, Q. Huang, G.F. Murphy, M.H. Frank, and N.Y. Frank ABCB5 identifies a therapy-refractory tumor cell population in colorectal cancer patients Cancer Res. 71 15 2011 5307 5316
123. J.D. Wolchok, B. Neyns, G. Linette, S. Negrier, J. Lutzky, L. Thomas, W. Waterfield, D. Schadendorf, M. Smylie, T. Guthrie Jr., J.J. Grob, J. Chesney, K. Chin, K. Chen, A. Hoos, S.J. O'Day, and C. Lebbe Ipilimumab monotherapy in patients with pretreated advanced melanoma: a randomised, double-blind, multicentre, phase 2, dose-ranging study Lancet Oncol. 11 2 2010 155 164
124. N.S. Wolf, A. Kone, G.V. Priestley, and S.H. Bartelmez In vivo and in vitro characterization of long-term repopulating primitive hematopoietic cells isolated by sequential Hoechst 33342-rhodamine 123 FACS selection Exp. Hematol. 21 5 1993 614 622
125. J. Yang, M.A. Price, G.Y. Li, M. Bar-Eli, R. Salgia, R. Jagedeeswaran, J.H. Carlson, S. Ferrone, E.A. Turley, and J.B. McCarthy Melanoma proteoglycan modifies gene expression to stimulate tumor cell motility, growth, and epithelial-to-mesenchymal transition Cancer Res. 69 19 2009 7538 7547
126. Q.L. Ying, J. Nichols, E.P. Evans, and A.G. Smith Changing potency by spontaneous fusion Nature 416 6880 2002 545 548
127. F. Yu, H. Yao, P. Zhu, X. Zhang, Q. Pan, C. Gong, Y. Huang, X. Hu, F. Su, J. Lieberman, and E. Song Let-7 regulates self renewal and tumorigenicity of breast cancer cells Cell 131 6 2007 1109 1123
128. S. Zhang, H. Guo, D. Zhang, W. Zhang, X. Zhao, Z. Ren, and B. Sun Microcirculation patterns in different stages of melanoma growth Oncol. Rep. 15 1 2006 15 20
129. S. Zhang, M. Li, Y. Gu, Z. Liu, S. Xu, Y. Cui, and B. Sun Thalidomide influences growth and vasculogenic mimicry channel formation in melanoma J. Exp. Clin. Cancer Res. 27 2008 60
130. S. Zhou, J.D. Schuetz, K.D. Bunting, A.M. Colapietro, J. Sampath, J.J. Morris, I. Lagutina, G.C. Grosveld, M. Osawa, H. Nakauchi, and B.P. Sorrentino The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype Nat. Med. 7 9 2001 1028 1034
131. J.M. Zijlmans, J.W. Visser, K. Kleiverda, P.M. Kluin, R. Willemze, and W.E. Fibbe Modification of rhodamine staining allows identification of hematopoietic stem cells with preferential short-term or long-term bone marrow-repopulating ability Proc. Natl. Acad. Sci. USA 92 19 1995 8901 8905