Spontaneous tumour regression in keratoacanthomas is driven by Wnt/retinoic acid signalling cross-talk

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zito, Giovanni ^a   Saotome, Ichiko ^a   Liu, Zongzhi ^a   Ferro, Enrico G ^a   Sun, Thomas Y ^a   Nguyen, Don X ^a   Bilguvar, Kaya ^a   Ko, Christine J ^b   Greco, Valentina ^a,b  

^a YALE CANCER CENTER   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID; WNT PROTEIN;

CANCER; CELL ORGANELLE; INHIBITION; ORGANIC ACID; PHYSIOLOGY; REGRESSION ANALYSIS; SIGNALING; TUMOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HAIR FOLLICLE; HUMAN; KERATOACANTHOMA; MOUSE; NONHUMAN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKIN CARCINOMA; TUMOR DIFFERENTIATION; TUMOR GROWTH; TUMOR REGRESSION; WNT SIGNALING PATHWAY; ANIMAL; CYTOLOGY; DISEASE MODEL; METABOLISM; REMISSION; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; STEM CELL;

ANIMALS; CARCINOMA, SQUAMOUS CELL; DISEASE MODELS, ANIMAL; HAIR FOLLICLE; KERATOACANTHOMA; MICE; REMISSION, SPONTANEOUS; SKIN NEOPLASMS; STEM CELLS; TRETINOIN; WNT SIGNALING PATHWAY;

EID: 84897068274     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4543     Document Type: Article

References (69)

1. Hamid, Y. & Poller, D. N. Spontaneous regression of renal cell carcinoma: a pitfall in diagnosis of renal lesions. J. Clin. Pathol. 51, 334-336 (1998).
2. Drobyski, W. R. & Qazi, R. Spontaneous regression in non-Hodgkin's lymphoma: clinical and pathogenetic considerations. Am. J. Hematol. 31, 138-141 (1989).
3. Nakagawara, A. Molecular basis of spontaneous regression of neuroblastoma: role of neurotrophic signals and genetic abnormalities. Hum. Cell 11, 115-124 (1998).
4. Ko, C. J. Keratoacanthoma: facts and controversies. Clin. Dermatol. 28, 254-261 (2010).
5. Blessing, K., Nafussi, A. & Gordon, P. M. The regressing keratoacanthoma. Histopathology 24, 381-384 (1994).
6. Weedon, D., Malo, J., Brooks, D. &Williamson, R. Keratoacanthoma: is it really a variant of squamous cell carcinoma? ANZ J. Surg. 80, 129-130 (2010).
7. Cribier, B., Asch, P. & Grosshans, E. Differentiating squamous cell carcinoma from keratoacanthoma using histopathological criteria. Is it possible? A study of 296 cases. Dermatology 199, 208-212 (1999).
8. Bayer-Garner, I. B., Ivan, D., Schwartz, M. R. & Tschen, J. A. The immunopathology of regression in benign lichenoid keratosis, keratoacanthoma and halo nevus. Clin. Med. Res. 2, 89-97 (2004).
9. Corominas, M. et al. Oncogene involvement in tumor regression: H-ras activation in the rabbit keratoacanthoma model. Oncogene 6, 645-651 (1991).
10. Corominas, M. et al. RAS activation in human tumors and in animal model systems. Environ. Health Perspect. 93, 19-25 (1991).
11. Ramselaar, C. G., Ruitenberg, E. J. & Kruizinga, W. Regression of induced keratoacanthomas in anagen (hair growth phase) skin grafts in mice. Cancer Res. 40, 1668-1673 (1980).
12. Greco, V. et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155-169 (2009).
13. Hardy, M. H. The secret life of the hair follicle. Trends Genet. 8, 55-61 (1992).
14. Van Mater, D., Kolligs, F. T., Dlugosz, A. A. & Fearon, E. R. Transient activation of beta-catenin signalling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev. 17, 1219-1224 (2003).
15. Lowry, W. E. et al. Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev. 19, 1596-1611 (2005).
16. Myung, P. S., Takeo, M., Ito, M. & Atit, R. P. Epithelial Wnt ligand secretion is required for adult hair follicle growth and regeneration. J. Investig. Dermatol. 133, 31-41 (2013).
17. Jho, E. H. et al. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183 (2002).
18. Kaufman, C. K. et al. GATA-3: an unexpected regulator of cell lineage determination in skin. Genes Dev. 17, 2108-2122 (2003).
19. van Amerongen, R. & Nusse, R. Towards an integrated view of Wnt signaling in development. Development 136, 3205-3214 (2009).
20. Shtutman, M. et al. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc. Natl Acad. Sci. USA 96, 5522-5527 (1999).
21. Gat, U., DasGupta, R., Degenstein, L. & Fuchs, E. De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell 95, 605-614 (1998).
22. Lo Celso, C., Prowse, D. M. & Watt, F. M. Transient activation of beta-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 131, 1787-1799 (2004).
23. Chapellier, B. et al. Physiological and retinoid-induced proliferations of epidermis basal keratinocytes are differently controlled. EMBO J. 21, 3402-3413 (2002).
24. Foitzik, K., Spexard, T., Nakamura, M., Halsner, U. & Paus, R. Towards dissecting the pathogenesis of retinoid-induced hair loss: all-trans retinoic acid induces premature hair follicle regression (catagen) by upregulation of transforming growth factor-beta2 in the dermal papilla. J. Investig. Dermatol. 124, 1119-1126 (2005).
25. Barker, N. et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608-611 (2009).
26. Proffitt, K. D. et al. Pharmacological inhibition of the Wnt acyltransferase PORCN prevents growth of WNT-driven mammary cancer. Cancer Res. 73, 502-507 (2013).
27. Beronja, S. et al. RNAi screens in mice identify physiological regulators of oncogenic growth. Nature 501, 185-190 (2013).
28. Di Piazza, M., Nowell, C. S., Koch, U., Durham, A. D. & Radtke, F. Loss of cutaneous TSLP-dependent immune responses skews the balance of inflammation from tumor protective to tumor promoting. Cancer Cell 22, 479-493 (2012).
29. Malanchi, I. et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 452, 650-653 (2008).
30. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
31. Schoop, V. M., Mirancea, N. & Fusenig, N. E. Epidermal organization and differentiation of HaCaT keratinocytes in organotypic coculture with human dermal fibroblasts. J. Investig. Dermatol. 112, 343-353 (1999).
32. Ferrer-Vaquer, A. et al. A sensitive and bright single-cell resolution live imaging reporter of Wnt/ss-catenin signaling in the mouse. BMC Dev. Biol. 10, 121 (2010).
33. Cruciat, C. M. & Niehrs, C. Secreted and transmembrane Wnt inhibitors and activators. Cold Spring Harb. Perspect. Biol. 5, a015081 (2013).
34. Chen, D., Jarrell, A., Guo, C., Lang, R. & Atit, R. Dermal beta-catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation. Development 139, 1522-1533 (2012).
35. Chen, B. et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 5, 100-107 (2009).
36. Vasioukhin, V., Degenstein, L., Wise, B. & Fuchs, E. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc. Natl Acad. Sci. USA 96, 8551-8556 (1999).
37. Harada, N. et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942 (1999).
38. Kumar, S. & Duester, G. Retinoic acid signaling in perioptic mesenchyme represses Wnt signaling via induction of Pitx2 and Dkk2. Dev. Biol. 340, 67-74 (2010).
39. Lapouge, G. et al. Identifying the cellular origin of squamous skin tumours. Proc. Natl Acad. Sci. USA 108, 7431-7436 (2011).
40. Bouras, T. et al. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 3, 429-441 (2008).
41. Nowak, J. A., Polak, L., Pasolli, H. A. & Fuchs, E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3, 33-43 (2008).
42. Wallace, L., Roberts-Thompson, L. & Reichelt, J. Deletion of K1/K10 does not impair epidermal stratification but affects desmosomal structure and nuclear integrity. J. Cell Sci. 125, 1750-1758 (2012).
43. Ito, M. et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat. Med. 11, 1351-1354 (2005).
44. Blagosklonny, M. V. Target for cancer therapy: proliferating cells or stem cells. Leukemia 20, 385-391 (2006).
45. Gupta, P. B. et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138, 645-659 (2009).
46. Hebbard, L. et al. Control of mammary tumor differentiation by SKI-606 (bosutinib). Oncogene 30, 301-312 (2011).
47. Fu, J. & Hsu, W. Epidermal Wnt controls hair follicle induction by orchestrating dynamic signaling crosstalk between the epidermis and dermis. J. Investig. Dermatol. 133, 890-898 (2013).
48. Chu, E. Y. et al. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 131, 4819-4829 (2004).
49. Okano, J. et al. Cutaneous retinoic acid levels determine hair follicle development and downgrowth. J. Biol. Chem. 287, 39304-39315 (2012).
50. Cho, K. W. et al. Retinoic acid signaling and the initiation of mammary gland development. Dev. Biol. 365, 259-266 (2012).
51. Schwitalla, S. et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152, 25-38 (2013).
52. Green, J. L. et al. Paracrine Wnt signaling both promotes and inhibits human breast tumor growth. Proc. Natl Acad. Sci. USA 110, 6991-6996 (2013).
53. Sinnberg, T. et al. Beta-catenin signaling increases during melanoma progression and promotes tumor cell survival and chemoresistance. PLoS One 6, e23429 (2011).
54. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
55. Trimboli, A. J. et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 461, 1084-1091 (2009).
56. Froeling, F. E. et al. Retinoic acid-induced pancreatic stellate cell quiescence reduces paracrine Wnt-beta-catenin signaling to slow tumor progression. Gastroenterology 141, 1486-1497 1497.e1-14 (2011).
57. Rompolas, P. et al. Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration. Nature 487, 496-499 (2012).
58. Crowe, D. L., Kim, R. & Chandraratna, R. A. Retinoic acid differentially regulates cancer cell proliferation via dose-dependent modulation of the mitogen-activated protein kinase pathway. Mol. Cancer Res. 1, 532-540 (2003).
59. Haydey, R. P., Reed, M. L., Dzubow, L. M. & Shupack, J. L. Treatment of keratoacanthomas with oral 13-cis-retinoic acid. New Engl. J. Med. 303, 560-562 (1980).
60. Aydin, F., Senturk, N., Sabanciler, E., Canturk, M. T. & Turanli, A. Y. A case of Ferguson-Smith type multiple keratoacanthomas associated with keratoacanthoma centrifugum marginatum: response to oral acitretin. Clin. Exp. Dermatol. 32, 683-686 (2007).
61. Lee, D. D. et al. Retinoid-responsive transcriptional changes in epidermal keratinocytes. J. Cell. Physiol. 220, 427-439 (2009).
62. Jiang, Y., Prunier, C. & Howe, P. H. The inhibitory effects of disabled-2 (Dab2) on Wnt signaling are mediated through Axin. Oncogene 27, 1865-1875 (2008).
63. Means, A. L., Xu, Y., Zhao, A., Ray, K. C. & Gu, G. A CK19(CreERT) knockin mouse line allows for conditional DNA recombination in epithelial cells in multiple endodermal organs. Genesis 46, 318-323 (2008).
64. Guasch, G. et al. Loss of TGFbeta signaling destabilizes homeostasis and promotes squamous cell carcinomas in stratified epithelia. Cancer Cell 12, 313-327 (2007).
65. Schober, M. & Fuchs, E. Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-beta and integrin/focal adhesion kinase (FAK) signaling. Proc. Natl Acad. Sci. USA 108, 10544-10549 (2011).
66. Nagy, A., Gertsenstein, M., Vintersten, K. & Behringer, R. Dewaxing and rehydrating sections prior to in situ hybridization. CSH Protoc. 2007, pdb prot4818 (2007).
67. Lohse, M. et al. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res. 40, W622-W627 (2012).
68. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
69. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).