Phenotype switching in melanoma: Implications for progression and therapy

Frontiers in Oncology

Volumn 5, Issue FEB, 2015, Pages

  Li, Frederic Zhentao ^a,b   Dhillon, Amardeep Singh ^a,b   Anderson, Robin L ^a,b   McArthur, Grant ^a,b   Ferrao, Petranel T ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

BRAF inhibition; EMT; Melanoma; metastasis; Phenotype switching; Resistance; RTK signaling

Indexed keywords

B RAF KINASE; BETA CATENIN; CATECHIN; DABRAFENIB; EPIGALLOCATECHIN GALLATE; METHOTREXATE; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; NERVE CELL ADHESION MOLECULE; OSTEONECTIN; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR; UVOMORULIN; VEMURAFENIB;

BONE MARROW PROGENITOR CELL; BREAST CARCINOMA; CANCER GROWTH; CANCER THERAPY; CELL INVASION; CELL PROLIFERATION; COLORECTAL CANCER; DOWN REGULATION; EPITHELIAL CANCER CELL LINE; EPITHELIAL MESENCHYMAL TRANSITION; GENE MUTATION; GENE SEQUENCE; GENE SWITCHING; GENETIC TRANSCRIPTION; HUMAN; IMMUNOHISTOCHEMISTRY; INVASIVE CARCINOMA; MELANOMA; METASTASIS; NERVE CELL PLASTICITY; NEURAL CREST CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SHORT SURVEY; TUMOR CELL; TUMOR GROWTH;

EID: 84923622377     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2015.00031     Document Type: Short Survey

References (77)

1. American Cancer Society. Cancer Facts and Figures. Atlanta, GA: American Cancer Society (2014). Available from: http://www.cancer.org/acs/groups/content/research/documents/webcontent/acspc-042151.pdf
2. Micheli A, Ciampichini R, Oberaigner W, Ciccolallo L, de Vries E, Izarzugaza I, et al. The advantage of women in cancer survival: an analysis of EUROCARE-4 data. Eur J Cancer (2009) 45(6):1017-27. doi: 10.1016/j.ejca.2008.11.008
3. Lucas R. Global Burden of Disease of Solar Ultraviolet Radiation, Environmental Burden of Disease Series. Geneva: World Health Organisation (2006).
4. Clark WH Jr., Elder DE, Guerry D IV, Epstein MN, Greene MH, Van Horn M. A study of tumor progression: the precursor lesions of superficial spreading and nodular melanoma. Hum Pathol (1984) 15(12):1147-65. doi:10.1016/S0046-8177(84)80310-X
5. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer (2002) 2(6):442-54. doi:10.1038/nrc822
6. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, et al. Variable ß-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci U S A (2001) 98(18):10356-61. doi:10.1073/pnas.171610498
7. Perl A-K, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature (1998) 392(6672):190-3. doi:10.1038/32433
8. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer (2007) 7(6):415-28. doi:10.1038/nrc2131
9. Thiery JP, Acloque H, Huang RYJ, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell (2009) 139(5):871-90. doi:10.1016/j.cell.2009.11.007
10. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, et al. The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol (2000) 2(2):84-9. doi:10.1038/35000034
11. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, et al. The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol (2000) 2(2):76-83. doi:10.1038/35010506
12. Bolós V, Peinado H, Pérez-Moreno MA, Fraga MF, Esteller M, Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci (2003) 116(3):499-511. doi:10.1242/jcs.00224
13. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, et al. The two-handed e box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell (2001) 7(6):1267-78. doi:10.1016/S1097-2765(01)00260-X
14. Aigner K, Dampier B, Descovich L, Mikula M, Sultan A, Schreiber M, et al. The transcription factor ZEB1 ([delta]EF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene (2007) 26(49):6979-88. doi:10.1038/sj.onc.1210508
15. Pérez-Moreno MA, Locascio A, Rodrigo I, Dhondt G, Portillo F, Nieto MA, et al. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J Biol Chem (2001) 276(29):27424-31. doi:10.1074/jbc.M100827200
16. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell (2004) 117(7):927-39. doi:10.1016/j.cell.2004.06.006
17. Sánchez-Tilló E, de Barrios O, Siles L, Cuatrecasas M, Castells A, Postigo A. ß-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc Natl Acad Sci U S A (2011) 108(48):19204-9. doi:10.1073/pnas.1108977108
18. Grotegut S, von Schweinitz D, Christofori G, Lehembre F. Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J (2006) 25(15):3534-45. doi:10.1038/sj.emboj.7601213
19. Lo H-W, Hsu S-C, Xia W, Cao X, Shih J-Y, Wei Y, et al. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res (2007) 67(19):9066-76. doi:10.1158/0008-5472.CAN-07-0575
20. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol (2006) 7(2):131-42. doi:10.1038/nrm1835
21. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell (2008) 14(6):818-29. doi:10.1016/j.devcel.2008.05.009
22. Baker CV, Bronner-Fraser M, Le Douarin NM, Teillet MA. Early- and late-migrating cranial neural crest cell populations have equivalent developmental potential in vivo. Development (1997) 124(16):3077-87.
23. Bennett DC. How to make a melanoma: what do we know of the primary clonal events? Pigment Cell Melanoma Res (2008) 21(1):27-38. doi:10.1111/j.1755-148X.2007.00433.x
24. Alonso SR, Tracey L, Ortiz P, Pérez-Gómez B, Palacios J, Pollán M, et al. A high-throughput study in melanoma identifies epithelial-mesenchymal transition as a major determinant of metastasis. Cancer Res (2007) 67(7):3450-60. doi:10.1158/0008-5472.CAN-06-3481
25. Hoek KS, Eichhoff OM, Schlegel NC, Döbbeling U, Kobert N, Schaerer L, et al. In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res (2008) 68(3):650-6. doi:10.1158/0008-5472.CAN-07-2491
26. Huang RYJ, Wong MK, Tan TZ, Kuay KT, Ng AHC, Chung VY, et al. An EMT spectrum defines an anoikis-resistant and spheroidogenic intermediate mesenchymal state that is sensitive to e-cadherin restoration by a src-kinase inhibitor, saracatinib (AZD0530). Cell Death Dis (2013) 4:e915. doi:10.1038/cddis.2013.442
27. Vandamme N, Berx G. Melanoma cells revive an embryonic transcriptional network to dictate phenotypic heterogeneity. Front Oncol (2014) 4:352. doi:10.3389/fonc.2014.00352
28. Caramel J, Papadogeorgakis E, Hill L, Browne Gareth J, Richard G, Wierinckx A, et al. A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma. Cancer Cell (2013) 24(4):466-80. doi:10.1016/j.ccr.2013.08.018
29. Denecker G, Vandamme N, Akay O, Koludrovic D, Taminau J, Lemeire K, et al. Identification of a ZEB2-MITF-ZEB1 transcriptional network that controls melanogenesis and melanoma progression. Cell Death Differ (2014) 21(8):1250-61. doi:10.1038/cdd.2014.44
30. Tomita K, van Bokhoven A, van Leenders GJLH, Ruijter ETG, Jansen CFJ, Bussemakers MJG, et al. Cadherin switching in human prostate cancer progression. Cancer Res (2000) 60(13):3650-4.
31. Krengel S, Grotelüschen F, Bartsch S, Tronnier M. Cadherin expression pattern in melanocytic tumors more likely depends on the melanocyte environment than on tumor cell progression. J Cutan Pathol (2004) 31(1):1-7. doi:10.1046/j.0303-6987.2004.0106.x
32. Fenouille N, Tichet M, Dufies M, Pottier A, Mogha A, Soo JK, et al. The epithelial-mesenchymal transition (EMT) regulatory factor SLUG (SNAI2) is a downstream target of SPARC and AKT in promoting melanoma cell invasion. PLoS One (2012) 7(7):e40378. doi:10.1371/journal.pone.0040378
33. Wels C, Joshi S, Koefinger P, Bergler H, Schaider H. Transcriptional activation of ZEB1 by slug leads to cooperative regulation of the epithelial-mesenchymal transition-like phenotype in melanoma. J Invest Dermatol (2011) 131(9):1877-85. doi:10.1038/jid.2011.142
34. Onken MD, Ehlers JP, Worley LA, Makita J, Yokota Y, Harbour JW. Functional gene expression analysis uncovers phenotypic switch in aggressive uveal melanomas. Cancer Res (2006) 66(9):4602-9. doi:10.1158/0008-5472.CAN-05-4196
35. Hoek KS, Goding CR. Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res (2010) 23(6):746-59. doi:10.1111/j.1755-148X.2010.00757.x
36. Kim K, Lu Z, Hay ED. Direct evidence for a role of ß-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol Int (2002) 26(5):463-76. doi:10.1006/cbir.2002.0901
37. Eichhoff OM, Weeraratna A, Zipser MC, Denat L, Widmer DS, Xu M, et al. Differential LEF1 and TCF4 expression is involved in melanoma cell phenotype switching. Pigment Cell Melanoma Res (2011) 24(4):631-42. doi:10.1111/j.1755-148X.2011.00871.x
38. Larue L, Delmas V. The WNT/Beta-catenin pathway in melanoma. Front Biosci (2006) 11:733-42. doi:10.2741/1831
39. Levy C, Khaled M, Fisher DE. MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol Med (2006) 12(9):406-14. doi:10.1016/j.molmed.2006.07.008
40. Steingrímsson E, Copeland NG, Jenkins NA. Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet (2004) 38(1):365-411. doi:10.1146/annurev.genet.38.072902.092717
41. Loercher AE, Tank EMH, Delston RB, Harbour JW. MITF links differentiation with cell cycle arrest in melanocytes by transcriptional activation of INK4A. J Cell Biol (2005) 168(1):35-40. doi:10.1083/jcb.200410115
42. Wellbrock C, Rana S, Paterson H, Pickersgill H, Brummelkamp T, Marais R. Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PLoS One (2008) 3(7):e2743. doi:10.1371/journal.pone.0002734
43. Carreira S, Goodall J, Denat L, Rodriguez M, Nuciforo P, Hoek KS, et al. Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev (2006) 20(24):3426-39. doi:10.1101/gad.406406
44. Dissanayake SK, Wade M, Johnson CE, O'Connell MP, Leotlela PD, French AD, et al. The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J Biol Chem (2007) 282(23):17259-71. doi:10.1074/jbc.M700075200
45. Sáez-Ayala M, Montenegro MF, Sánchez-Del-Campo L, Fernández-Pérez MP, Chazarra S, Freter R, et al. Directed phenotype switching as an effective antimelanoma strategy. Cancer Cell (2013) 24(1):105-19. doi:10.1016/j.ccr.2013.05.009
46. O'Connell MP, Marchbank K, Webster MR, Valiga AA, Kaur A, Vultur A, et al. Hypoxia induces phenotypic plasticity and therapy resistance in melanoma via the tyrosine kinase receptors ROR1 and ROR2. Cancer Discov (2013) 3(12):1378-93. doi:10.1158/2159-8290.CD-13-0005
47. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med (2012) 18(6):883-91. doi:10.1038/nm.2753
48. Chalkiadakia G, Nikitovica D, Berdiakia A, Sifakia M, Krasagakis K, Katonisc P, et al. Fibroblast growth factor-2 modulates melanoma adhesion and migration through a syndecan-4-dependent mechanism. Int J Biochem Cell Biol (2009) 41(6):1323-31. doi:10.1016/j.biocel.2008.11.008
49. Gaggioli C, Deckert M, Robert G, Abbe P, Batoz M, Ehrengruber MU, et al. HGF induces fibronectin matrix synthesis in melanoma cells through MAP kinase-dependent signaling pathway and induction of Egr-1. Oncogene (2005) 24(8):1423-33. doi:10.1038/sj.onc.1208318
50. All-Ericsson C, Girnita L, Seregard S, Bartolazzi A, Jager MJ, Larsson O. Insulin-like Growth factor-1 receptor in Uveal melanoma: a predictor for metastatic disease and a potential therapeutic target. Invest Ophthalmol Vis Sci (2002) 43(1):1-8.
51. Cornell RA, Eisen JS. Notch in the pathway: the roles of notch signaling in neural crest development. Semin Cell Dev Biol (2005) 16(6):663-72. doi:10.1016/j.semcdb.2005.06.009
52. Wu J, Yang J, Klein PS. Neural crest induction by the canonical Wnt pathway can be dissociated from anterior-posterior neural patterning in Xenopus. Dev Biol (2005) 279(1):220-32. doi:10.1016/j.ydbio.2004.12.016
53. Takebe N, Harris PJ, Warren RQ, Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol (2011) 8(2):97-106. doi:10.1038/nrclinonc.2010.196
54. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature (2002) 417(6892):949-54. doi:10.1038/nature00766
55. Ball NJ, Yohn JJ, Morelli JG, Norris DA, Golitz LE, Hoeffler JP. Ras mutations in human melanoma: a marker of malignant progression. J Invest Dermatol (1994) 102(3):285-90. doi:10.1111/1523-1747.ep12371783
56. Lin K, Baritaki S, Militello L, Malaponte G, Bevelacqua Y, Bonavida B. The role of B-RAF mutations in melanoma and the induction of EMT via dysregulation of the NF-?B/Snail/RKIP/PTEN Circuit. Genes Cancer (2010) 1(5):409-20. doi:10.1177/1947601910373795
57. Massoumi R, Kuphal S, Hellerbrand C, Haas B, Wild P, Spruss T, et al. Down-regulation of CYLD expression by Snail promotes tumor progression in malignant melanoma. J Exp Med (2009) 206(1):221-32. doi:10.1084/jem.20082044
58. Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during snail-induced EMT of cancer cells. Cancer Cell (2009) 15(3):195-206. doi:10.1016/j.ccr.2009.01.023
59. Bracher A, Cardona AS, Tauber S, Fink AM, Steiner A, Pehamberger H, et al. Epidermal growth factor facilitates melanoma lymph node metastasis by influencing tumor lymphangiogenesis. J Invest Dermatol (2013) 133(1):230-8. doi:10.1038/jid.2012.272
60. Koefinger P, Wels C, Joshi S, Damm S, Steinbauer E, Beham-Schmid C, et al. The cadherin switch in melanoma instigated by HGF is mediated through epithelial-mesenchymal transition regulators. Pigment Cell Melanoma Res (2011) 24(2):382-5. doi:10.1111/j.1755-148X.2010.00807.x
61. Kapaettu S, Gang LI, Bhavesh V, Jiri K, Meenhard H. Insulin-like growth factor-I-induced migration of melanoma cells is mediated by interleukin-8 induction. Cell Growth Differ (2002) 13(2):87-93.
62. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-[beta] family signalling. Nature (2003) 425(6958):577-84. doi:10.1038/nature02006
63. Zavadil J, Bottinger EP. TGF-[beta] and epithelial-to-mesenchymal transitions. Oncogene (2005) 24(37):5764-74. doi:10.1038/sj.onc.1208927
64. Morita T, Mayanagi T, Sobue K. Dual roles of myocardin-related transcription factors in epithelial-mesenchymal transition via slug induction and actin remodeling. J Cell Biol (2007) 179(5):1027-42. doi:10.1083/jcb.200708174
65. Huang S, Hölzel M, Knijnenburg T, Schlicker A, Roepman P, McDermott U, et al. MED12 controls the response to multiple cancer drugs through regulation of TGF-ß receptor signaling. Cell (2012) 151(5):937-50. doi:10.1016/j.cell.2012.10.035
66. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med (2010) 363(9):809-19. doi:10.1056/NEJMoa1002011
67. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med (2011) 364(26):2507-16. doi:10.1056/NEJMoa1103782
68. Hauschild A, Grob J-J, Demidov LV, Jouary T, Gutzmer R, Millward M, et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial. Lancet (2012) 380(9839):358-65. doi:10.1016/S0140-6736(12)60868-X
69. Sullivan RJ, Flaherty KT. Resistance to BRAF-targeted therapy in melanoma. Eur J Cancer (2013) 49(6):1297-304. doi:10.1016/j.ejca.2012.11.019
70. Kaplon J, Zheng L, Meissl K, Chaneton B, Selivanov VA, Mackay G, et al. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature (2013) 498(7452):109-12. doi:10.1038/nature12154
71. Ma X-H, Piao S-F, Dey S, McAfee Q, Karakousis G, Villanueva J, et al. Targeting ER stress-induced autophagy overcomes BRAF inhibitor resistance in melanoma. J Clin Invest (2014) 124(3):1406-17. doi:10.1172/JCI70454
72. Parmenter TJ, Kleinschmidt M, Kinross KM, Bond ST, Li J, Kaadige MR, et al. Response of BRAF-mutant melanoma to BRAF inhibition is mediated by a network of transcriptional regulators of glycolysis. Cancer Discov (2014) 4(4):423-33. doi:10.1158/2159-8290.CD-13-0440
73. Singh T, Katiyar SK. Green tea catechins reduce invasive potential of human melanoma cells by targeting COX-2, PGE2 receptors and epithelial-to-mesenchymal transition. PLoS One (2011) 6(10):e25224. doi:10.1371/journal.pone.0025224
74. Anastas JN, Kulikauskas RM, Tamir T, Rizos H, Long GV, von Euw EM, et al. WNT5A enhances resistance of melanoma cells to targeted BRAF inhibitors. J Clin Invest (2014) 124(7):2877-90. doi:10.1172/JCI70156
75. Girotti MR, Pedersen M, Sanchez-Laorden B, Viros A, Turajlic S, Niculescu-Duvaz D, et al. Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov (2013) 3(2):158-67. doi:10.1158/2159-8290.CD-12-0386
76. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J, et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature (2012) 487(7408):500-4. doi:10.1038/nature11183
77. Vella LJ. The emerging role of exosomes in epithelial-mesenchymal-transition in cancer. Front Oncol (2014) 4:361. doi:10.3389/fonc.2014.00361