Display options
Cite
Haridas P, McGovern JA, McElwain SDL, et al. Quantitative comparison of the spreading and invasion of radial growth phase and metastatic melanoma cells in a three-dimensional human skin equivalent model. PeerJ. 2017;5:e3754doi: 10.7717/peerj.3754.
Haridas, P., McGovern, J. A., McElwain, S. D. L., & Simpson, M. J. (2017). Quantitative comparison of the spreading and invasion of radial growth phase and metastatic melanoma cells in a three-dimensional human skin equivalent model. PeerJ, 5e3754. https://doi.org/10.7717/peerj.3754
Haridas, Parvathi, et al. "Quantitative comparison of the spreading and invasion of radial growth phase and metastatic melanoma cells in a three-dimensional human skin equivalent model." PeerJ vol. 5 (2017): e3754. doi: https://doi.org/10.7717/peerj.3754
Haridas P, McGovern JA, McElwain SDL, Simpson MJ. Quantitative comparison of the spreading and invasion of radial growth phase and metastatic melanoma cells in a three-dimensional human skin equivalent model. PeerJ. 2017 Sep 05;5:e3754. doi: 10.7717/peerj.3754. eCollection 2017. PMID: 28890854; PMCID: PMC5590551.
Copy Download .nbib Format: NLM
Share it on

PeerJ. 2017 Sep 05;5:e3754. doi: 10.7717/peerj.3754. eCollection 2017.

Quantitative comparison of the spreading and invasion of radial growth phase and metastatic melanoma cells in a three-dimensional human skin equivalent model.

PeerJ

Parvathi Haridas, Jacqui A McGovern, Sean D L McElwain, Matthew J Simpson

Affiliations

  1. Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Queensland, Australia.
  2. School of Mathematical Sciences, Queensland University of Technology, Brisbane, Queensland, Australia.

PMID: 28890854 PMCID: PMC5590551 DOI: 10.7717/peerj.3754

Abstract

BACKGROUND: Standard two-dimensional (2D) cell migration assays do not provide information about vertical invasion processes, which are critical for melanoma progression. We provide information about three-dimensional (3D) melanoma cell migration, proliferation and invasion in a 3D melanoma skin equivalent (MSE) model. In particular, we pay careful attention to compare the structure of the tissues in the MSE with similarly-prepared 3D human skin equivalent (HSE) models. The HSE model is identically prepared to the MSE model except that melanoma cells are omitted. Using the MSE model, we examine melanoma migration, proliferation and invasion from two different human melanoma cell lines. One cell line, WM35, is associated with the early phase of the disease where spreading is thought to be confined to the epidermis. The other cell line, SK-MEL-28, is associated with the later phase of the disease where spreading into the dermis is expected.

METHODS: 3D MSE and HSE models are constructed using human de-epidermised dermis (DED) prepared from skin tissue. Primary fibroblasts and primary keratinocytes are used in the MSE and HSE models to ensure the formation of a stratified epidermis, with a well-defined basement membrane. Radial spreading of cells across the surface of the HSE and MSE models is observed. Vertical invasion of melanoma cells downward through the skin is observed and measured using immunohistochemistry. All measurements of invasion are made at day 0, 9, 15 and 20, providing detailed time course data.

RESULTS: Both HSE and MSE models are similar to native skin

DISCUSSION: The MSE and HSE models are a reliable platform for studying melanoma invasion in a 3D tissue that is similar to native human skin. Interestingly, we find that the WM35 cell line, that is thought to be associated with radial spreading only, is able to invade into the dermis. The vertical invasion of melanoma cells into the dermal region appears to be associated with a localised disruption of the basement membrane. Presenting our results in terms of time course data, along with images and quantitative measurements of the depth of invasion extends previous 3D work that has often been reported without these details.

Keywords: Cancer; Cell line; Cell migration; Invasion; Melanoma; Metastasis; Skin cancer; Skin equivalent model; Skin model; Three dimensional model

Conflict of interest statement

The authors declare there are no competing interests.

References

  1. Melanoma Res. 2000 Apr;10(2):127-40 - PubMed
  2. PeerJ. 2016 Feb 15;4:e1689 - PubMed
  3. J Theor Biol. 2017 Jun 21;423:13-25 - PubMed
  4. Adv Wound Care (New Rochelle). 2014 Mar 1;3(3):272-280 - PubMed
  5. Exp Cell Res. 2007 Jun 10;313(10):2050-62 - PubMed
  6. Dermatol Res Pract. 2010;2010:null - PubMed
  7. Healthcare (Basel). 2013 Dec 23;2(1):27-46 - PubMed
  8. J Med Life. 2014 Oct-Dec;7(4):572-6 - PubMed
  9. Sci Rep. 2016 Apr 18;6:24569 - PubMed
  10. Eur J Cell Biol. 2015 Nov;94(11):483-512 - PubMed
  11. Mol Cell. 2015 Aug 20;59(4):664-76 - PubMed
  12. Transplantation. 2006 Jun 27;81(12):1668-76 - PubMed
  13. Pathology. 2013 Aug;45(5):443-52 - PubMed
  14. J Clin Aesthet Dermatol. 2014 Jun;7(6):13-24 - PubMed
  15. Steroids. 2010 Mar;75(3):230-9 - PubMed
  16. Cancer Res. 2008 Jul 15;68(14):5743-52 - PubMed
  17. Oncogenesis. 2014 Jul 07;3:e110 - PubMed
  18. Cancer Res. 1996 Jul 1;56(13):3075-86 - PubMed
  19. J Cell Biochem. 2007 Jul 1;101(4):805-15 - PubMed
  20. BMC Med. 2012 Mar 02;10:23 - PubMed
  21. Melanoma Res. 2010 Oct;20(5):372-80 - PubMed
  22. J R Soc Interface. 2014 Aug 6;11(97):20140325 - PubMed
  23. Am J Pathol. 2000 Jan;156(1):193-200 - PubMed
  24. Mutat Res. 2013 Jan-Mar;752(1):10-24 - PubMed
  25. JAMA. 2000 Aug 16;284(7):886-9 - PubMed
  26. Front Genet. 2013 May 31;4:97 - PubMed
  27. PLoS One. 2014 Apr 07;9(4):e94229 - PubMed
  28. Cell. 2000 Jan 7;100(1):57-70 - PubMed
  29. Cancers (Basel). 2010 Dec 30;3(1):126-63 - PubMed
  30. J Cell Physiol. 2010 Jan;222(1):38-41 - PubMed
  31. Br J Dermatol. 2013 Mar;168(3):496-503 - PubMed
  32. Oncotarget. 2015 Dec 1;6(38):40535-56 - PubMed
  33. Br J Dermatol. 2000 Feb;142(2):210-22 - PubMed
  34. Cancer Metastasis Rev. 1990 Sep;9(2):101-12 - PubMed
  35. PLoS One. 2013 Jun 24;8(6):e67389 - PubMed
  36. Proteomics. 2008 Nov;8(22):4733-47 - PubMed
  37. Ontogenez. 2013 May-Jun;44(3):186-202 - PubMed
  38. J Histochem Cytochem. 2008 Apr;56(4):347-58 - PubMed
  39. Clin Exp Metastasis. 2003;20(8):685-700 - PubMed
  40. Cell Death Dis. 2013 Jul 11;4:e719 - PubMed
  41. Clin Cancer Res. 2008 Oct 1;14(19):6193-7 - PubMed
  42. Melanoma Res. 2000 Oct;10(5):427-34 - PubMed
  43. J Clin Pathol. 2004 Aug;57(8):797-801 - PubMed
  44. Tissue Eng Part C Methods. 2010 Oct;16(5):1111-23 - PubMed
  45. Tissue Eng Part C Methods. 2014 Jul;20(7):588-98 - PubMed
  46. Am J Pathol. 1998 Nov;153(5):1435-42 - PubMed
  47. J Invest Dermatol. 2013 Jan;133(1):210-20 - PubMed
  48. Dev Dyn. 1993 Aug;197(4):255-67 - PubMed
  49. Oncotarget. 2015 Jun 30;6(18):15966-83 - PubMed
  50. PeerJ. 2013 Mar 05;1:e49 - PubMed
  51. Melanoma Res. 1997 Aug;7 Suppl 2:S35-42 - PubMed
  52. J Natl Cancer Inst. 2010 Aug 4;102(15):1148-59 - PubMed
  53. Mayo Clin Proc. 2006 Apr;81(4):500-7 - PubMed
  54. J Oral Maxillofac Pathol. 2015 Jan-Apr;19(1):64-8 - PubMed
  55. Pigment Cell Res. 2000;13 Suppl 8:68-72 - PubMed
  56. Scientifica (Cairo). 2013;2013:635203 - PubMed
  57. Cancer Res. 2008 May 15;68(10):3671-9 - PubMed
  58. J R Soc Interface. 2013 Feb 20;10(82):20130007 - PubMed
  59. Cell. 1975 Nov;6(3):331-43 - PubMed
  60. Nature. 2014 Sep 4;513(7516):105-9 - PubMed
  61. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3278-82 - PubMed
  62. PLoS One. 2016 Jun 07;11(6):e0156931 - PubMed
  63. Oncotarget. 2014 Aug 30;5(16):7051-64 - PubMed
  64. Int J Cancer. 2003 Sep 1;106(3):316-23 - PubMed
  65. Sci Rep. 2014 Jul 16;4:5713 - PubMed
  66. Br J Cancer. 2003 Nov 17;89(10):2004-15 - PubMed
  67. Lancet Oncol. 2013 Feb;14 (2):e60-9 - PubMed
  68. Proc Natl Acad Sci U S A. 2015 Apr 28;112(17 ):5366-71 - PubMed
  69. Cancer Res. 2005 Oct 1;65(19):8774-83 - PubMed
  70. Trends Cell Biol. 2015 Feb;25(2):92-9 - PubMed
  71. Pigment Cell Res. 2007 Jun;20(3):161-72 - PubMed
  72. J Biomech. 2016 May 24;49(8):1381-1387 - PubMed
  73. Oncol Lett. 2017 May;13(5):3787-3792 - PubMed
  74. J Invest Dermatol. 2008 Oct;128(10):2381-91 - PubMed
  75. Br J Dermatol. 1999 Nov;141(5):811-23 - PubMed
  76. N Engl J Med. 2006 Jul 6;355(1):51-65 - PubMed
  77. BMC Syst Biol. 2013 Dec 12;7:137 - PubMed
  78. Pharmacol Res. 2016 Sep;111:523-533 - PubMed
  79. Br J Cancer. 1991 Oct;64(4):631-44 - PubMed

Publication Types