Real-time cell cycle imaging during melanoma growth, invasion, and drug response

Pigment Cell and Melanoma Research

Volumn 27, Issue 5, 2014, Pages 764-776

  Haass, Nikolas K ^a,b,c,d   Beaumont, Kimberley A ^a,e   Hill, David S ^a,e   Anfosso, Andrea ^a,e   Mrass, Paulus ^a,e   Munoz, Marcia A ^a,e   Kinjyo, Ichiko ^a,e   Weninger, Wolfgang ^a,b,c  

^a CENTENARY INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cancer drug resistance; Fluorescent ubiquitination based cell cycle indicator; Invasion; Melanoma heterogeneity; Migration; Real time imaging; Tumor microenvironment

Indexed keywords

ANTINEOPLASTIC AGENT; FLUORESCENT DYE; UBIQUITIN;

ANIMAL; CANCER TRANSPLANTATION; CELL CYCLE; CELL CYCLE G1 PHASE; CELL HYPOXIA; CELL MOTION; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HUMAN; MELANOMA; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; FEMALE; FLUORESCENT DYES; G1 PHASE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MELANOMA; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; UBIQUITIN;

EID: 84907977588     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12274     Document Type: Article

References (44)

1. Aguirre-Ghiso, J.A. (2007). Models, mechanisms and clinical evidence for cancer dormancy. Nat. Rev. Cancer 7, 834-846.
2. Alexander, S., and Friedl, P. (2012). Cancer invasion and resistance: interconnected processes of disease progression and therapy failure. Trends Mol. Med. 18, 13-26.
3. Anada, T., Fukuda, J., Sai, Y., and Suzuki, O. (2012). An oxygen-permeable spheroid culture system for the prevention of central hypoxia and necrosis of spheroids. Biomaterials 33, 8430-8441.
4. Bagrodia, S., Smeal, T., and Abraham, R.T. (2012). Mechanisms of intrinsic and acquired resistance to kinase-targeted therapies. Pigment Cell Melanoma Res. 25, 819-831.
5. Beaumont, K.A., Mohana-Kumaran, N., and Haass, N.K. (2014). Modeling melanoma in vitro and in vivo. Healthcare 2, 27-46.
6. Brandner, J.M., and Haass, N.K. (2013). Melanoma's connections to the tumour microenvironment. Pathology 45, 443-452.
7. Carreira, S., Goodall, J., Denat, L., Rodriguez, M., Nuciforo, P., Hoek, K.S., Testori, A., Larue, L., and Goding, C.R. (2006). Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev. 20, 3426-3439.
8. Durand, R.E. (1982). Use of Hoechst 33342 for cell selection from multicell systems. J. Histochem. Cytochem. 30, 117-122.
9. Groebe, K., and Mueller-Klieser, W. (1991). Distributions of oxygen, nutrient, and metabolic waste concentrations in multicellular spheroids and their dependence on spheroid parameters. Eur. Biophys. J. 19, 169-181.
10. Haass, N.K., and Schumacher, U. (2014). Melanoma never says die. Exp. Dermatol. [Epub ahead of print].
11. Haass, N.K., Sproesser, K., Nguyen, T.K., Contractor, R., Medina, C.A., Nathanson, K.L., Herlyn, M., and Smalley, K.S. (2008). The mitogen-activated protein/extracellular signal-regulated kinase kinase inhibitor AZD6244 (ARRY-142886) induces growth arrest in melanoma cells and tumor regression when combined with docetaxel. Clin. Cancer Res. 14, 230-239.
12. Hanahan, D., and Weinberg, R.A. (2000). The hallmarks of cancer. Cell 100, 57-70.
13. Hanahan, D., and Weinberg, R.A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
14. Hoek, K.S., and Goding, C.R. (2010). Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res. 23, 746-759.
15. Hoek, K.S., Schlegel, N.C., Brafford, P. et al. (2006). Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res. 19, 290-302.
16. Hoek, K.S., Eichhoff, O.M., Schlegel, N.C., Dobbeling, U., Kobert, N., Schaerer, L., Hemmi, S., and Dummer, R. (2008). In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res. 68, 650-656.
17. Lee, J.T., Li, L., Brafford, P.A. et al. (2010). PLX4032, a potent inhibitor of the B-Raf V600E oncogene, selectively inhibits V600E-positive melanomas. Pigment Cell Melanoma Res. 23, 820-827.
18. Li, J.L., Goh, C.C., Keeble, J.L., Qin, J.S., Roediger, B., Jain, R., Wang, Y., Chew, W.K., Weninger, W., and Ng, L.G. (2012). Intravital multiphoton imaging of immune responses in the mouse ear skin. Nat. Protoc. 7, 221-234.
19. Lucas, K.M., Mohana-Kumaran, N., Lau, D., Zhang, X.D., Hersey, P., Huang, D.C., Weninger, W., Haass, N.K., and Allen, J.D. (2012). Modulation of NOXA and MCL-1 as a strategy for sensitizing melanoma cells to the BH3-Mimetic ABT-737. Clin. Cancer Res. 18, 783-795.
20. Minchinton, A.I., and Tannock, I.F. (2006). Drug penetration in solid tumours. Nat. Rev. Cancer 6, 583-592.
21. Mrass, P., Takano, H., Ng, L.G. et al. (2006). Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J. Exp. Med. 203, 2749-2761.
22. Nowell, P.C. (1976). The clonal evolution of tumor cell populations. Science 194, 23-28.
23. O'Connell, M.P., Marchbank, K., Webster, M.R. et al. (2013). Hypoxia induces phenotypic plasticity and therapy resistance in melanoma via the tyrosine kinase receptors ROR1 and ROR2. Cancer Discov. 3, 1378-1393.
24. Pavey, S., Spoerri, L., Haass, N.K., and Gabrielli, B. (2013). DNA repair and cell cycle checkpoint defects as drivers and therapeutic targets in melanoma. Pigment Cell Melanoma Res. 26, 805-816.
25. Reya, T., Morrison, S.J., Clarke, M.F., and Weissman, I.L. (2001). Stem cells, cancer, and cancer stem cells. Nature 414, 105-111.
26. Roesch, A., Fukunaga-Kalabis, M., Schmidt, E.C., Zabierowski, S.E., Brafford, P.A., Vultur, A., Basu, D., Gimotty, P., Vogt, T., and Herlyn, M. (2010). A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141, 583-594.
27. Sakaue-Sawano, A., Kurokawa, H., Morimura, T. et al. (2008). Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487-498.
28. Santiago-Walker, A., Li, L., Haass, N.K., and Herlyn, M. (2009). Melanocytes: from morphology to application. Skin Pharmacol. Physiol. 22, 114-121.
29. Shackleton, M. (2010). Moving targets that drive cancer progression. N. Engl. J. Med. 363, 885-886.
30. Smalley, K.S., Brafford, P., Haass, N.K., Brandner, J.M., Brown, E., and Herlyn, M. (2005). Up-regulated expression of zonula occludens protein-1 in human melanoma associates with N-cadherin and contributes to invasion and adhesion. Am. J. Pathol. 166, 1541-1554.
31. Smalley, K.S., Haass, N.K., Brafford, P.A., Lioni, M., Flaherty, K.T., and Herlyn, M. (2006). Multiple signaling pathways must be targeted to overcome drug resistance in cell lines derived from melanoma metastases. Mol. Cancer Ther. 5, 1136-1144.
32. Smalley, K.S., Contractor, R., Haass, N.K. et al. (2007a). An organometallic protein kinase inhibitor pharmacologically activates p53 and induces apoptosis in human melanoma cells. Cancer Res. 67, 209-217.
33. Smalley, K.S., Contractor, R., Haass, N.K., Lee, J.T., Nathanson, K.L., Medina, C.A., Flaherty, K.T., and Herlyn, M. (2007b). Ki67 expression levels are a better marker of reduced melanoma growth following MEK inhibitor treatment than phospho-ERK levels. Br. J. Cancer 96, 445-449.
34. Smalley, K.S., Lioni, M., Noma, K., Haass, N.K., and Herlyn, M. (2008). In vitro three-dimensional tumor microenvironment models for anticancer drug discovery. Expert Opin. Drug Discov. 3, 1-10.
35. Somasundaram, R., Villanueva, J., and Herlyn, M. (2012). Intratumoral heterogeneity as a therapy resistance mechanism: role of melanoma subpopulations. Adv. Pharmacol. 65, 335-359.
36. Tong, P.L., Qin, J., Cooper, C.L., Lowe, P.M., Murrell, D.F., Kossard, S., Ng, L.G., Roediger, B., Weninger, W., and Haass, N.K. (2013). A quantitative approach to histopathological dissection of elastin-related disorders using multiphoton microscopy. Br. J. Dermatol. 169, 869-879.
37. Tsai, J., Lee, J.T., Wang, W. et al. (2008). Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc. Natl Acad. Sci. U. S. A. 105, 3041-3046.
38. Tsao, H., Chin, L., Garraway, L.A., and Fisher, D.E. (2012). Melanoma: from mutations to medicine. Genes Dev. 26, 1131-1155.
39. Villanueva, J., and Herlyn, M. (2008). Melanoma and the tumor microenvironment. Curr. Oncol. Rep. 10, 439-446.
40. Vultur, A., Villanueva, J., Krepler, C. et al. (2014). MEK inhibition affects STAT3 signaling and invasion in human melanoma cell lines. Oncogene 33, 1850-1861.
41. Wagle, N., Emery, C., Berger, M.F. et al. (2011). Dissecting therapeutic resistance to RAF inhibition in melanoma by tumor genomic profiling. J. Clin. Oncol. 29, 3085-3096.
42. Widmer, D.S., Hoek, K.S., Cheng, P.F., Eichhoff, O.M., Biedermann, T., Raaijmakers, M.I., Hemmi, S., Dummer, R., and Levesque, M.P. (2013). Hypoxia contributes to melanoma heterogeneity by triggering HIF1alpha-dependent phenotype switching. J. Invest. Dermatol. 133, 2436-2443.
43. Zhuang, L., Lee, C.S., Scolyer, R.A., Mccarthy, S.W., Palmer, A.A., Zhang, X.D., Thompson, J.F., Bron, L.P., and Hersey, P. (2005). Activation of the extracellular signal regulated kinase (ERK) pathway in human melanoma. J. Clin. Pathol. 58, 1163-1169.
44. Zipser, M.C., Eichhoff, O.M., Widmer, D.S. et al. (2011). A proliferative melanoma cell phenotype is responsive to RAF/MEK inhibition independent of BRAF mutation status. Pigment Cell Melanoma Res. 24, 326-333.