Skip to main content

Skin Stem Cells in Cancer

  • Chapter
  • First Online:
Cancer Stem Cells: New Horizons in Cancer Therapies
  • 543 Accesses

Abstract

Stem cells (SCs) are responsible for maintaining and regenerating tissues and show unique defining characteristics, including self-renewal, asymmetrical cell division, low proliferation rate, and clonogenic potential. Niches of epidermal SCs have been identified in the bulge of hair follicles, the basal layer of the interfollicular epidermis, and the base of sebaceous glands. Accumulating evidence suggests that multipotent bulge cells generate hair follicles under physiological conditions and regenerate the epidermis and sebaceous glands in response to skin injury. In contrast, SCs of the interfollicular epidermis and sebaceous glands are lineage specific and generate their respective tissues without recruiting SCs from the bulge compartment. Cancer stem cells (CSCs) represent a class of tumor cells exhibiting stem cell-like properties and ability to initiate tumors. They are derived from SCs or from non-stem cells that acquire self-renewal potential. Likely SCs, CSCs express regulatory factors of self-renewal, such as SOX2, MYC, and OCT4, and some common “stemness” pathways, such as Wnt signaling. In contrast, they could not be multipotent and lead to single lineage tumors, such as squamous cell carcinoma (SCC) (epidermal lineage), various follicular tumor types (hair follicle lineage), and sebaceous gland tumors (sebaceous lineage). Currently, several studies on CSC biology have been performed to develop new targeted therapies for patients with skin tumors with poor prognoses.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Bickenbach JR (1981) Identification and behavior of label-retaining cells in oral mucosa and skin. J Dent Res 60(Spec C):1611–1620. https://doi.org/10.1177/002203458106000311011

    Article  PubMed  Google Scholar 

  2. Blanpain C, Fuchs E (2006) Epidermal stem cells of the skin. Annu Rev Cell Dev Biol 22:339–373. https://doi.org/10.1146/annurev.cellbio.22.010305.104357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Tumbar T, Guasch G, Greco V et al (2004) Defining the epithelial stem cell niche in skin. Science 303:359–363. https://doi.org/10.1126/science.1092436

    Article  CAS  PubMed  Google Scholar 

  4. Levy V, Lindon C, Harfe BD, Morgan BA (2005) Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell 9:855–861. https://doi.org/10.1016/j.devcel.2005.11.003

    Article  CAS  PubMed  Google Scholar 

  5. Watt FM (1998) Epidermal stem cells: markers, patterning and the control of stem cell fate. Philos Trans R Soc B Biol Sci 353:831–837. https://doi.org/10.1098/rstb.1998.0247

    Article  CAS  Google Scholar 

  6. Bickenbach JR, Stern MM (2005) Plasticity of epidermal stem cells: survival in various environments. Stem Cell Rev 1:71–77. https://doi.org/10.1385/scr:1:1:071

    Article  CAS  PubMed  Google Scholar 

  7. Kaur P, Li A (2000) Adhesive properties of human basal epidermal cells: an analysis of keratinocyte stem cells, transit amplifying cells, and postmitotic differentiating cells. J Invest Dermatol 114:413–420. https://doi.org/10.1046/j.1523-1747.2000.00884.x

    Article  CAS  PubMed  Google Scholar 

  8. Schmidt-Ullrich R, Paus R (2005) Molecular principles of hair follicle induction and morphogenesis. Bioessays 27:247–261. https://doi.org/10.1002/bies.20184

    Article  CAS  PubMed  Google Scholar 

  9. Murone M, Rosenthal A, De Sauvage FJ (1999) Sonic hedgehog signaling by the patched-smoothened receptor complex. Curr Biol 9:76–84. https://doi.org/10.1016/S0960-9822(99)80018-9

    Article  CAS  PubMed  Google Scholar 

  10. Eckert R, Adhikary G, Balasubramanian S et al (2014) Biochemistry of epidermal stem cells. Am J Biosci 2:22–34. https://doi.org/10.1016/j.bbagen.2012.07.002.Biochemistry

    Article  Google Scholar 

  11. Lowell S, Jones P, Le Roux I et al (2000) Stimulation of human epidermal differentiation by Delta-notch signalling at the boundaries of stem-cell clusters. Curr Biol 10:491–500. https://doi.org/10.1016/S0960-9822(00)00451-6

    Article  CAS  PubMed  Google Scholar 

  12. Yi R, Poy MN, Stoffel M, Fuchs E (2008) A skin microRNA promotes differentiation by repressing “stemness”. Nature 452:225–229. https://doi.org/10.1038/nature06642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Su X, Chakravarti D, Cho MS et al (2010) TAp63 suppresses metastasis through coordinate regulation of dicer and miRNAs. Nature 467:986–990. https://doi.org/10.1038/nature09459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhang L, Stokes N, Polak L, Fuchs E (2011) Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment. Cell Stem Cell 8:294–308. https://doi.org/10.1016/j.stem.2011.01.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Myung P, Ito M (2012) Dissecting the bulge in hair regeneration. J Clin Invest 122:448–454. https://doi.org/10.1172/JCI57414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ohyama M, Terunuma A, Tock CL et al (2006) Characterization and isolation of stem cell–enriched human hair follicle bulge cells. J Clin Invest 116:249–260. https://doi.org/10.1007/978-1-61779-815-3_24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bose A, Teh MT, Mackenzie IC, Waseem A (2013) Keratin K15 as a biomarker of epidermal stem cells. Int J Mol Sci 14:19385–19398. https://doi.org/10.3390/ijms141019385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Inoue K, Aoi N, Sato T et al (2009) Differential expression of stem-cell-associated markers in human hair follicle epithelial cells. Lab Invest 89:844–856. https://doi.org/10.1038/labinvest.2009.48

    Article  CAS  PubMed  Google Scholar 

  19. Boehnke K, Falkowska-Hansen B, Stark HJ, Boukamp P (2012) Stem cells of the human epidermis and their niche: composition and function in epidermal regeneration and carcinogenesis. Carcinogenesis 33:1247–1258. https://doi.org/10.1093/carcin/bgs136

    Article  CAS  PubMed  Google Scholar 

  20. Trempus CS, Morris RJ, Ehinger M et al (2007) CD34 expression by hair follicle stem cells is required for skin tumor development in mice. Cancer Res 67:4173–4181. https://doi.org/10.1158/0008-5472.CAN-06-3128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Morris RJ, Liu Y, Marles L et al (2004) Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22:411–417. https://doi.org/10.1038/nbt950

    Article  CAS  PubMed  Google Scholar 

  22. Nijhof JGW, Braun KM, Giangreco A et al (2006) The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development 133:3027–3037. https://doi.org/10.1242/dev.02443

    Article  CAS  PubMed  Google Scholar 

  23. Jensen UB, Yan X, Triel C et al (2008) A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus. J Cell Sci 121:609–617. https://doi.org/10.1242/jcs.025502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jensen KB, Collins CA, Nascimento E et al (2009) Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 4:427–439. https://doi.org/10.1016/j.stem.2009.04.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Snippert HJ, Haegebarth A, Kasper M et al (2010) Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 327:1385–1389. https://doi.org/10.1126/science.1184733

    Article  CAS  PubMed  Google Scholar 

  26. Horsley V, O’Carroll D, Tooze R et al (2006) Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126:597–609. https://doi.org/10.1016/j.cell.2006.06.048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Sulewski R, Kirsner RS (2010) The multipotent nature of hair bulge cells. J Invest Dermatol 130:1198. https://doi.org/10.1038/jid.2010.81

    Article  CAS  PubMed  Google Scholar 

  28. Deng W, Han QIN, Liao L et al (2005) Engrafted bone marrow-derived Flk-1. Tissue Eng 11:110–119

    Article  CAS  Google Scholar 

  29. Baxter MA (2004) Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22:675–682. https://doi.org/10.1634/stemcells.22-5-675

    Article  CAS  PubMed  Google Scholar 

  30. Morris RJ, Fischer SM, Slaga TJ (1986) Evidence that a slowly cycling subpopulation of adult murine epidermal cells retains carcinogen. Cancer Res 46:3061–3066

    CAS  PubMed  Google Scholar 

  31. Jamieson CHM, Ailles LE, Dylla SJ et al (2004) Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 351:657–667. https://doi.org/10.1056/NEJMoa040258

    Article  CAS  PubMed  Google Scholar 

  32. Owens DM, Watt FM (2003) Contribution of stem cells and differentiated cells to epidermal tumours. Nat Rev Cancer 3:444–451. https://doi.org/10.1038/nrc1096

    Article  CAS  PubMed  Google Scholar 

  33. Roberts KJ, Kershner AM, Beachy PA (2017) The stromal niche for epithelial stem cells: a template for regeneration and a brake on malignancy. Cancer Cell 32:404–410. https://doi.org/10.1016/j.ccell.2017.08.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lander AD, Kimble J, Clevers H et al (2012) What does the concept of the stem cell niche really mean today? BMC Biol 10:1–15. https://doi.org/10.1186/1741-7007-10-19

    Article  Google Scholar 

  35. Shin K, Lim A, Zhao C et al (2014) Re: Hedgehog signaling restrains bladder cancer progression by eliciting stromal production of urothelial differentiation factors. J Urol 19426:521–533. https://doi.org/10.1016/j.juro.2015.04.038

    Article  Google Scholar 

  36. Sekulic A, Migden MR, Oro AE et al (2012) Efficacy and safety of vismodegib in advanced basal-cell carcinoma. N Engl J Med 366:2171–2179. https://doi.org/10.1056/NEJMoa1113713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Song IY, Balmain A (2015) Cellular reprogramming in skin cancer. Semin Cancer Biol 32:32–39. https://doi.org/10.1111/mec.13536.Application

    Article  PubMed  Google Scholar 

  38. Oshimori N, Oristian D, Fuchs E (2015) TGF-β promotes heterogeneity and drug resistance in squamous cell carcinoma. Cell 160:963–976. https://doi.org/10.1016/j.physbeh.2017.03.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Beck B, Driessens G, Goossens S et al (2011) A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 478:399–403. https://doi.org/10.1038/nature10525

    Article  CAS  PubMed  Google Scholar 

  40. Siegle JM, Basin A, Sastre-Perona A et al (2015) SOX2 is a cancer-specific regulator of tumor initiating potential in cutaneous squamous cell carcinoma. Nat Commun 5:139. https://doi.org/10.1016/j.physbeh.2017.03.040

    Article  CAS  Google Scholar 

  41. White RA, Neiman JM, Reddi A et al (2013) Epithelial stem cell mutations that promote squamous cell carcinoma metastasis. J Clin Invest 123:4390–4404. https://doi.org/10.1172/JCI65856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Fuchs E (2009) Finding One’s Niche in the skin. Cell Stem Cell 4:499–502. https://doi.org/10.1016/j.stem.2009.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bose B, Shenoy SP (2014) Stem cell versus cancer and cancer stem cell: intricate balance decides their respective usefulness or harmfulness in the biological system. J Stem Cell Res Ther 4. https://doi.org/10.4172/2157-7633.1000173

  44. Forni MF, Lobba ARM, Ferreira AHP, Sogayar MC (2015) Simultaneous isolation of three different stem cell populations from murine skin. PLoS One 10:1–16. https://doi.org/10.1371/journal.pone.0140143

    Article  CAS  Google Scholar 

  45. Jamora C, DasGupta R, Kocieniewski P, Fuchs E (2003) Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422:317–322. https://doi.org/10.1038/nature01458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kretzschmar K, Watt FM (2014) Markers of epidermal stem cell subpopulations. Cold Spring Harb Perspect Med 4:1–14

    Article  Google Scholar 

  47. Martin MT, Vulin A, Hendry JH (2016) Human epidermal stem cells: role in adverse skin reactions and carcinogenesis from radiation. Mutat Res/Rev Mutat Res 770:349–368. https://doi.org/10.1016/j.mrrev.2016.08.004

    Article  CAS  Google Scholar 

  48. Jang BG, Lee C, Kim HS et al (2017) Distinct expression profile of stem cell markers, LGR5 and LGR6, in basaloid skin tumors. Virchows Arch 470:301–310. https://doi.org/10.1007/s00428-016-2061-3

    Article  CAS  PubMed  Google Scholar 

  49. Wong VW, Levi B, Rajadas J et al (2012) Stem cell niches for skin regeneration. Int J Biomater 2012:1. https://doi.org/10.1155/2012/926059

    Article  CAS  Google Scholar 

  50. Yang R, Wang J, Chen X et al (2020) Epidermal stem cells in wound healing and regeneration. Stem Cells Int 2020:1–14. https://doi.org/10.1155/2020/9148310

    Article  CAS  Google Scholar 

  51. Klimczak A, Kozlowska U (2015) Mesenchymal stromal cells and tissue-specific progenitor cells: their role in tissue homeostasis. Stem Cells Int 2016:4285215. https://doi.org/10.1155/2016/4285215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Kang HY, Hwang JS, Lee JY et al (2006) The dermal stem cell factor and c-kit are overexpressed in melasma. Br J Dermatol 154:1094–1099. https://doi.org/10.1111/j.1365-2133.2006.07179.x

    Article  CAS  PubMed  Google Scholar 

  53. Trempus CS, Morris RJ, Bortner CD et al (2003) Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J Invest Dermatol 120:501–511. https://doi.org/10.1046/j.1523-1747.2003.12088.x

    Article  CAS  PubMed  Google Scholar 

  54. Youssef M, Cuddihy A, Darido C (2017) Long-lived epidermal cancer-initiating cells. Int J Mol Sci 18:18. https://doi.org/10.3390/ijms18071369

    Article  CAS  Google Scholar 

  55. Cangkrama M, Ting SB, Darido C (2013) Stem cells behind the barrier. Int J Mol Sci 14:13670–13686. https://doi.org/10.3390/ijms140713670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Fluhr JW, Kao J, Jain M et al (2001) Generation of free fatty acids from phospholipids regulates stratum corneum acidification and integrity. J Invest Dermatol 117:44–51. https://doi.org/10.1046/j.0022-202X.2001.01399.x

    Article  CAS  PubMed  Google Scholar 

  57. Darido C, Georgy SR, Wilanowski T et al (2011) Targeting of the tumor suppressor GRHL3 by a miR-21-dependent proto-oncogenic network results in PTEN loss and tumorigenesis. Cancer Cell 20:635–648. https://doi.org/10.1016/j.ccr.2011.10.014

    Article  CAS  PubMed  Google Scholar 

  58. Erb P, Ji J, Kump E et al (2008) Apoptosis and pathogenesis of melanoma and nonmelanoma skin cancer. Adv Exp Med Biol 624:283–295. https://doi.org/10.1007/978-0-387-77574-6_22

    Article  CAS  PubMed  Google Scholar 

  59. Al-Hajj M, Clarke MF (2004) Self-renewal and solid tumor stem cells. Oncogene 23:7274–7282. https://doi.org/10.1038/sj.onc.1207947

    Article  CAS  PubMed  Google Scholar 

  60. Patel SS, Shah KA, Shah MJ et al (2014) Cancer stem cells and stemness markers in oral squamous cell carcinomas. Asian Pac J Cancer Prev 15:8549–8556. https://doi.org/10.7314/APJCP.2014.15.20.8549

    Article  PubMed  Google Scholar 

  61. Roudi R, Korourian A, Shariftabrizi A, Madjd Z (2015) Differential expression of cancer stem cell markers ALDH1 and CD133 in various lung cancer subtypes. Cancer Invest 33:294–302. https://doi.org/10.3109/07357907.2015.1034869

    Article  CAS  PubMed  Google Scholar 

  62. Prince ME, Sivanandan R, Kaczorowski A et al (2007) Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. PNAS 104:973–978. https://doi.org/10.1073/pnas.0610117104

    Article  CAS  PubMed  Google Scholar 

  63. Bergoglio V, Larcher F, Chevallier-Lagente O et al (2007) Safe selection of genetically manipulated human primary keratinocytes with very high growth potential using CD24. Mol Ther 15:2186–2193. https://doi.org/10.1038/sj.mt.6300292

    Article  CAS  PubMed  Google Scholar 

  64. Sellheyer K (2011) Basal cell carcinoma: cell of origin, cancer stem cell hypothesis and stem cell markers. Br J Dermatol 164:696–711. https://doi.org/10.1111/j.1365-2133.2010.10158.x

    Article  CAS  PubMed  Google Scholar 

  65. Tanese K, Fukuma M, Yamada T et al (2008) G-protein-coupled receptor GPR49 is up-regulated in basal cell carcinoma and promotes cell proliferation and tumor formation. Am J Pathol 173:835–843. https://doi.org/10.2353/ajpath.2008.071091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Perego M, Tortoreto M, Tragni G et al (2010) Heterogeneous phenotype of human melanoma cells with in vitro and in vivo features of tumor-initiating cells. J Invest Dermatol 130:1877–1886. https://doi.org/10.1038/jid.2010.69

    Article  CAS  PubMed  Google Scholar 

  67. Peterson SC, Eberl M, Vagnozzi AN et al (2015) Basal cell carcinoma preferentially arises from stem cells within hair follicle and mechanosensory niches. Cell Stem Cell 16:400–412. https://doi.org/10.1016/j.physbeh.2017.03.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Schober M, Fuchs E (2011) Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-β and integrin/focal adhesion kinase (FAK) signaling. Proc Natl Acad Sci U S A 108:10544–10549. https://doi.org/10.1073/pnas.1107807108

    Article  PubMed  PubMed Central  Google Scholar 

  69. Jian Z, Strait A, Jimeno A, Wang X (2017) Cancer stem cells in squamous cell carcinoma. J Invest Dermatol 137:31–37. https://doi.org/10.1016/j.jid.2016.07.033.Cancer

    Article  CAS  PubMed  Google Scholar 

  70. Kim BG, Kim MI, Lee JW et al (2015) Expression of cancer stem cell marker during 4-nitroquinoline 1-oxide-induced rat tongue carcinogenesis. Int J Oral Maxillofac Surg 44:e244–e245. https://doi.org/10.1016/j.ijom.2015.08.184

    Article  Google Scholar 

  71. Lang D, Mascarenhas JB, Shea CR (2013) Melanocytes, melanocyte stem cells, and melanoma stem cells. Clin Dermatol 31:166–178. https://doi.org/10.1016/j.clindermatol.2012.08.014

    Article  PubMed  PubMed Central  Google Scholar 

  72. Al-Garf AK, Ibrahim Assaf M, Abdel-Gawad Nofal A, Abdel-Shafy AS (2013) Expression of microRNAs in basal cell carcinoma. Br J Dermatol 19:290–303. https://doi.org/10.1111/j.1365-2133.2012.11022.x

    Article  CAS  Google Scholar 

  73. Lapouge G, Beck B, Nassar D et al (2012) Skin squamous cell carcinoma propagating cells increase with tumour progression and invasiveness. EMBO J 31:4563–4575. https://doi.org/10.1038/emboj.2012.312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Civenni G, Walter A, Kobert N et al (2011) Human CD271-positive melanoma stem cells associated with metastasis establish tumor heterogeneity and long-term growth. Cancer Res 71:3098–3109. https://doi.org/10.1158/0008-5472.CAN-10-3997

    Article  CAS  PubMed  Google Scholar 

  75. Katoh M (2017) Canonical and non-canonical WNT signaling in cancer stem cells and their niches: cellular heterogeneity, omics reprogramming, targeted therapy and tumor plasticity (review). Int J Oncol 51:1357–1369. https://doi.org/10.3892/ijo.2017.4129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Olivero C, Morgan H, Patel GK (2018) Identification of human cutaneous squamous cell carcinoma Cancer stem cells. Methods Mol Biol 1879:415–433

    Article  Google Scholar 

  77. Venkatesh V, Nataraj R, Thangaraj GS et al (2018) Targeting notch signalling pathway of cancer stem cells. Stem Cell Investig 5:5. https://doi.org/10.21037/sci.2018.02.02

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Stumpfova M, Ratner D, Desciak EB et al (2010) The immunosuppressive surface ligand CD200 augments the metastatic capacity of squamous cell carcinoma. Cancer Res 70:2962–2972. https://doi.org/10.1158/0008-5472.CAN-09-4380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Kumar D, Gorain M, Kundu G, Kundu GC (2017) Therapeutic implications of cellular and molecular biology of cancer stem cells in melanoma. Mol Cancer 16:1–18. https://doi.org/10.1186/s12943-016-0578-3

    Article  CAS  Google Scholar 

  80. Callahan CA, Ofstad T, Horng L et al (2004) MIM/BEG4, a Sonic that potentiates Gli-dependent transcription. Genes Dev 18:2724–2729. https://doi.org/10.1101/gad.1221804.2724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Boumahdi S, Driessens G, Lapouge G et al (2014) SOX2 controls tumour initiation and cancer stem-cell functions in squamous-cell carcinoma. Nature 511:246–250. https://doi.org/10.1038/nature13305

    Article  CAS  PubMed  Google Scholar 

  82. Santini R, Pietrobono S, Pandolfi S et al (2014) SOX2 regulates self-renewal and tumorigenicity of human melanoma-initiating cells. Oncogene 33:4697–4708. https://doi.org/10.1038/onc.2014.71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Moloney FJ, Comber H, O’Lorcain P et al (2006) A population-based study of skin cancer incidence and prevalence in renal transplant recipients. Br J Dermatol 154:498–504. https://doi.org/10.1111/j.1365-2133.2005.07021.x

    Article  CAS  PubMed  Google Scholar 

  84. Chang CC, Campoli M, Ferrone S (2003) HLA class I defects in malignant lesions: what have we learned? Keio J Med 52:220–229. https://doi.org/10.2302/kjm.52.220

    Article  CAS  PubMed  Google Scholar 

  85. Yesantharao P, Wang W, Ioannidis NM et al (2017) Cutaneous squamous cell cancer (cSCC) risk and the human leukocyte antigen (HLA) system. Hum Immunol 78:327–335. https://doi.org/10.1016/j.humimm.2017.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Chen AC, Halliday GM, Damian DL (2013) Non-melanoma skin cancer: carcinogenesis and chemoprevention. Pathology 45:331–341. https://doi.org/10.1097/PAT.0b013e32835f515c

    Article  CAS  PubMed  Google Scholar 

  87. Schwarz A, Noordegraaf M, Maeda A et al (2010) Langerhans cells are required for UVR-induced immunosuppression. J Invest Dermatol 130:1419–1427. https://doi.org/10.1038/jid.2009.429

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosa Di Liddo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Piccione, M., Di Liddo, R. (2020). Skin Stem Cells in Cancer. In: Pathak, S., Banerjee, A. (eds) Cancer Stem Cells: New Horizons in Cancer Therapies. Springer, Singapore. https://doi.org/10.1007/978-981-15-5120-8_6

Download citation

Publish with us

Policies and ethics