Sonic hedgehog signaling in basal cell nevus syndrome

Cancer Research

Volumn 74, Issue 18, 2014, Pages 4967-4975

  Athar, Mohammad ^a   Li, Changzhao ^a   Kim, Arianna L ^b   Spiegelman, Vladimir S ^c   Bickers, David R ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; SONIC HEDGEHOG PROTEIN;

ANIMAL; BASAL CELL NEVUS SYNDROME; CELL GROWTH; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BASAL CELL NEVUS SYNDROME; CELL GROWTH PROCESSES; DISEASE MODELS, ANIMAL; HEDGEHOG PROTEINS; HUMANS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84907484153     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1666     Document Type: Review

References (90)

1. Rogers HW, Weinstock MA, Harris AR, Hinckley MR, Feldman SR, Fleischer AB, et al. Incidence estimate of nonmelanoma skin cancer in the United States, 2006. Arch Dermatol 2010;146:283-7.
2. Karia PS, Han J, Schmults CD. Cutaneous squamous cell carcinoma: estimated incidence of disease, nodal metastasis, and deaths from disease in the United States, 2012. J Am Acad Dermatol 2013;68:957-66.
3. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014;64:9-29.
4. Epstein EH. Basal cell carcinomas: attack of the hedgehog. Nat Rev Cancer 2008;8:743-54.
5. Kimonis VE, Mehta SG, Digiovanna JJ, Bale SJ, Pastakia B. Radiological features in 82 patients with nevoid basal cell carcinoma (NBCC or Gorlin) syndrome. Genet Med 2004;6:495-502.
6. Endo M, Fujii K, Sugita K, Saito K, Kohno Y, Miyashita T. Nationwide survey of nevoid basal cell carcinoma syndrome in Japan revealing the low frequency of basal cell carcinoma. Am J Med Genet Part A 2012;158A: 351-7.
7. Goldstein AM, Pastakia B, Di Giovanna JJ, Poliak S, Santucci S, Kase R, et al. Clinical findings in two African-American families with the nevoid basal cell carcinoma syndrome (NBCC). Am J Med Genet 1994;50:272-81.
8. Gailani MR, Bale SJ, Leffell DJ, Di Giovanna JJ, Peck GL, Poliak S, et al. Developmental defects in Gorlin syndrome related to a putative tumor-suppressor gene on chromosome 9. Cell 1992;69:111-7.
9. Kakanj P, Reuter K, Sequaris G, Wodtke C, Schettina P, Frances D, et al. Indian hedgehog controls proliferation and differentiation in skin tumorigenesis and protects against malignant progression. Cell Rep 2013;4:340-51.
10. Adolphe C, Narang M, Ellis T, Wicking C, Kaur P, Wainwright B. An in vivo comparative study of sonic, desert and Indian hedgehog reveals that hedgehog pathway activity regulates epidermal stem cell homeostasis. Development 2004;131:5009-19.
11. Brunner M, Thurnher D, Pammer J, Heiduschka G, Petzelbauer P, Schmid C, et al. Expression of hedgehog signaling molecules in Merkel cell carcinoma. Head Neck 2010;32:333-40.
12. Athar M, Tang X, Lee JL, Kopelovich L, Kim AL. Hedgehog signalling in skin development and cancer. Exp Dermatol 2006;15:667-77.
13. Zackheim HS. The origin of experimental basal cell epitheliomas in the rat. J Invest Dermatol 1962;38:57-64.
14. Sellheyer K. Basal cell carcinoma: cell of origin, cancer stem cell hypothesis, and stem cell markers. Br J Dermatol 2011;164:696-711.
15. Zackheim HS. Origin of the human basal cell epithelioma. J Invest Dermatol 1963;40:283-97.
16. Cotsarelis G, Sun TT, Lavker RM. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 1990;61:1329-37.
17. Youssef KK, Lapouge G, Bouvree K, Rorive S, Brohee S, Appelstein O, et al. Adult interfolliculartumour-initiating cells are reprogrammed into an embryonic hair follicle progenitor-like fate during basal cell carcinoma initiation. Nat Cell Bio 2012;14:1282-94.
18. Wang GY, Wang J, Mancianti ML, Epstein EH Jr. Basal cell carcinomas arise from hair follicle stem cells in Ptch1 (+/-) mice. Cancer Cell 2011;19:114-24.
19. Grachtchouk M, Pero J, Yang SH, Ermilov AN, Michael LE, Wang A, et al. Basal cell carcinomas in mice arise from hairfollicle stem cells and multiple epithelial progenitor populations. J Clin Invest 2011;121:1768-81.
20. Amakye D, Jagani Z, Dorsch M. Unraveling the therapeutic potential of the Hedgehog pathway in cancer. Nat Med 2013;19:1410-22.
21. Merchant JL, Saqui-Salces M. Inhibition of Hedgehog signaling in the gastrointestinal tract: targeting the cancer microenvironment. Cancer Treat Rev 2014;40:12-21.
22. Ok CY, Singh RR, Vega F. Aberrant activation of the hedgehog signaling pathway in malignant hematological neoplasms. Am J Pathol 2012;180:2-11.
23. Lauth M, Toftgard R. Non-canonical activation of GLI transcription factors: implications for targeted anti-cancer therapy. Cell Cycle 2007;6:2458-63.
24. Bertrand FE, Angus CW, Partis WJ, Sigounas G. Developmental pathways in colon cancer: crosstalk between WNT, BMP, Hedgehog, and Notch. Cell Cycle 2012;11:4344-51.
25. Javelaud D, Pierrat MJ, Mauviel A. Crosstalk between TGF-beta and hedgehog signaling in cancer. FEBS Lett 2012;586:2016-25.
26. Schnidar H, Eberl M, Klingler S, Mangelberger D, Kasper M, Hauser-Kronberger C, et al. Epidermal growth factor receptor signaling synergizes with Hedgehog/GLI in oncogenic transformation via activation of the MEK/ERK/JUN pathway. Cancer Res 2009;69:1284-92.
27. Yang SH, Andl T, Grachtchouk V, Wang A, Liu J, Syu LJ, et al. Pathological responses to oncogenic Hedgehog signaling in skin are dependent on canonical Wnt/beta3-catenin signaling. Nat Genet 2008;40:1130-5.
28. Kim JH, Shin HS, Lee SH, Lee I, Lee YS, Park JC, et al. Contrasting activity of Hedgehog and Wnt pathways according to gastric cancer cell differentiation: relevance of crosstalk mechanisms. Cancer Sci 2010;101:328-35.
29. Ulloa F, Itasaki N, Briscoe J. Inhibitory Gli3 activity negatively regulates Wnt/beta-catenin signaling. Curr Biol 2007;17:545-50.
30. Noubissi FK, Kim T, Kawahara TN, Aughenbaugh WD, Berg E, Longley BJ, et al. Role of CRD-BP in the growth of human basal cell carcinoma cells. J Invest Dermatol 2014;134:1718-24.
31. Wang Y, Ding Q, Yen CJ, Xia W, Izzo JG, Lang JY, et al. The crosstalk of mTOR/S6K1 and Hedgehog pathways. Cancer Cell 2012;21:374-87.
32. Kaylani SZ, Xu J, Srivastava RK, Kopelovich L, Pressey JG, Athar M. Rapamycin targeting mTOR and hedgehog signaling pathways blocks human rhabdomyosarcoma growth in xenograft murine model. Biochem Biophys Res Commun 2013;435:557-61.
33. Li ZJ, Nieuwenhuis E, Nien W, Zhang X, Zhang J, Puviindran V, et al. Kif7 regulates Gli2 through Sufu-dependent and -independent functions during skin development and tumorigenesis. Development 2012;139:4152-61.
34. Varjosalo M, Bjorklund M, Cheng F, Syvanen H, Kivioja T, Kilpinen S, et al. Application of active and kinase-deficient kinome collection for identification of kinases regulating hedgehog signaling. Cell 2008;133:537-48.
35. Maloverjan A, Piirsoo M, Michelson P, Kogerman P, Osterlund T. Identification of a novel serine/threonine kinase ULK3 as a positive regulator of Hedgehog pathway. Exp Cell Res 2010;316:627-37.
36. Evangelista M, Lim TY, Lee J, Parker L, Ashique A, Peterson AS, et al. Kinome siRNA screen identifies regulators of ciliogenesis and hedgehog signal transduction. Sci Signal 2008;1: ra7.
37. Yoo YA, Kang MH, Lee HJ, Kim BH, Park JK, Kim HK, et al. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res 2011;71:7061-70.
38. McCusker M, Basset-Seguin N, Dummer R, Lewis K, Schadendorf D, Sekulic A, et al. Metastatic basal cell carcinoma: prognosis dependent on anatomic site and spread of disease. Eur J Cancer 2014;50:774-83.
39. De Craene B, Denecker G, Vermassen P, Taminau J, Mauch C, Derore A, et al. Epidermal Snail expression drives skin cancer initiation and progression through enhanced cytoprotection, epidermal stem/progenitor cell expansion, and enhanced metastatic potential. Cell Death Differ 2014;21:310-20.
40. Croyle MJ, Lehman JM, O'Connor AK, Wong SY, Malarkey EB, Iribarne D, et al. Role of epidermal primary cilia in the homeostasis of skin and hair follicles. Development 2011;138:1675-85.
41. Nozawa YI, Lin C, Chuang PT. Hedgehog signaling from the primary cilium to the nucleus: an emerging picture of ciliary localization, trafficking, and transduction. Curr Opin Genet Dev 2013;23:429-37.
42. Tuson M, He M, Anderson KV. Protein kinase A acts at the basal body of the primary cilium to prevent Gli2 activation and ventralization of the mouse neural tube. Development 2011;138:4921-30.
43. Jiang J. Regulation of Hh/Gli signaling by dual ubiquitin pathways. Cell Cycle 2006;5:2457-63.
44. Baujat G, Le Merrer M. Ellis-van Creveld syndrome. Orphanet J Rare Dis 2007;2:27.
45. D'Asdia MC, Torrente I, Consoli F, Ferese R, Magliozzi M, Bernardini L, et al. Novel and recurrent EVC and EVC2 mutations in Ellis-van Creveld syndrome and Weyers acrofacial dyostosis. Eur J Med Genet 2013;56:80-7.
46. Ruiz-Perez VL, Goodship JA. Ellis-van Creveld syndrome and Weyers acrodental dysostosis are caused by cilia-mediated diminished response to hedgehog ligands. Am J Med Genet C Semin Med Genet 2009;151C: 341-51.
47. Dorn KV, Hughes CE, Rohatgi R. A Smoothened-Evc2 complex transduces the Hedgehog signal at primary cilia. Dev Cell 2012;23:823-35.
48. Kuzhandaivel A, Schultz SW, Alkhori L, Alenius M. Cilia-mediated hedgehog signaling in Drosophila. Cell Rep 2014;7:672-80.
49. Yang C, Chen W, Chen Y, Jiang J. Smoothened transduces Hedgehog signal by forming a complex with Evc/Evc2. Cell Res 2012;22:1593-604.
50. Pusapati GV, Hughes CE, Dorn KV, Zhang D, Sugianto P, Aravind L, et al. EFCAB7 and IQCE regulate hedgehog signaling by tethering the EVC-EVC2 complex to the base of primary cilia. Dev Cell 2014;28:483-96.
51. Delling M, De Caen PG, Doerner JF, Febvay S, Clapham DE. Primary cilia are specialized calcium signalling organelles. Nature 2013;504:311-4.
52. Oro AE, Higgins KM, Hu Z, Bonifas JM, Epstein EH Jr, Scott MP. Basal cell carcinomas in mice overexpressing sonic hedgehog. Science 1997;276:817-21.
53. Aszterbaum M, Epstein J, Oro A, Douglas V, Le Boit PE, Scott MP, et al. Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice. Nat Med 1999;5:1285-91.
54. Tang X, Kim AL, Feith DJ, Pegg AE, Russo J, Zhang H, et al. Ornithine decarboxylase is a target for chemoprevention of basal and squamous cell carcinomas in Ptch1+/-mice. J Clin Invest 2004;113:867-75.
55. Nitzki F, Becker M, Frommhold A, Schulz-Schaeffer W, Hahn H. Patched knockout mouse models of Basal cell carcinoma. J Skin Cancer 2012;2012:907543.
56. Colmont CS, Benketah A, Reed SH, Hawk NV, Telford WG, Ohyama M, et al. CD200-expressing human basal cell carcinoma cells initiate tumor growth. Proc Natl Acad Sci USA 2013;110:1434-9.
57. Sims-Mourtada J, Izzo JG, Ajani J, Chao KS. Sonic Hedgehog promotes multiple drug resistance by regulation of drug transport. Oncogene 2007;26:5674-9.
58. Blagosklonny MV. Teratogens as anti-cancer drugs. Cell Cycle 2005;4:1518-21.
59. Taipale J, Chen JK, Cooper MK, Wang B, Mann RK, Milenkovic L, et al. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 2000;406:1005-9.
60. Athar M, Li C, Tang X, Chi S, Zhang X, Kim AL, et al. Inhibition of smoothened signaling prevents ultraviolet B-induced basal cell carcinomas through regulation of Fas expression and apoptosis. Cancer Res 2004;64:7545-52.
61. Kimura H, Ng JM, Curran T. Transient inhibition of the Hedgehog pathway in young mice causes permanent defects in bone structure. Cancer Cell 2008;13:249-60.
62. Meyers-Needham M, Lewis JA, Gencer S, Sentelle RD, Saddoughi SA, Clarke CJ, et al. Off-target function of the Sonic hedgehog inhibitor cyclopamine in mediating apoptosis via nitric oxide-dependent neutral sphingomyelinase 2/ceramide induction. Mol Cancer Ther 2012;11:1092-102.
63. Curran T. Mouse models and mouse supermodels. EMBO Mol Med 2010;2:385-6; author reply 86-7.
64. Lipinski RJ, Hutson PR, Hannam PW, Nydza RJ, Washington IM, Moore RW, et al. Dose- and route-dependent teratogenicity, toxicity, and pharmacokinetic profiles of the hedgehog signaling antagonist cyclopamine in the mouse. Toxicol Sci 2008;104:189-97.
65. Vogt A, Chuang PT, Hebert J, Hwang J, Lu Y, Kopelovich L, et al. Immunoprevention of basal cell carcinomas with recombinant hedgehog-interacting protein. J Exp Med 2004;199:753-61.
66. Stanton BZ, Peng LF, Maloof N, Nakai K, Wang X, Duffner JL, et al. A small molecule that binds Hedgehog and blocks its signaling in human cells. Nat Chem Biol 2009;5:154-6.
67. Atwood SX, Li M, Lee A, Tang JY, Oro AE. GLI activation by atypical protein kinase C iota/lambda regulates the growth of basal cell carcinomas. Nature 2013;494:484-8.
68. Kim J, Tang JY, Gong R, Kim J, Lee JJ, Clemons KV, et al. Itraconazole, a commonly used antifungal that inhibits Hedgehog pathway activity and cancer growth. Cancer Cell 2010;17:388-99.
69. Kim DJ, Kim J, Spaunhurst K, Montoya J, Khodosh R, Chandra K, et al. Open-label, exploratory phase II trial of oral itraconazole for the treatment of basal cell carcinoma. J Clin Oncol 2014;32:745-51.
70. Kim J, Aftab BT, Tang JY, Kim D, Lee AH, Rezaee M, et al. Itraconazole and arsenic trioxide inhibit Hedgehog pathway activation and tumor growth associated with acquired resistance to smoothened antagonists. Cancer Cell 2013;23:23-34.
71. Kim J, Lee JJ, Kim J, Gardner D, Beachy PA. Arsenic antagonizes the Hedgehog pathway by preventing ciliary accumulation and reducing stability of the Gli2 transcriptional effector. Proc Natl Acad Sci U S A 2010;107:13432-7.
72. Beauchamp EM, Ringer L, Bulut G, Sajwan KP, Hall MD, Lee YC, et al. Arsenic trioxide inhibits human cancer cell growth and tumor development in mice by blocking Hedgehog/GLI pathway. J Clin Invest 2011;121:148-60.
73. Tang JY, Xiao TZ, Oda Y, Chang KS, Shpall E, Wu A, et al. Vitamin D3 nhibits hedgehog signaling and proliferation in murine Basal cell carcinomas. Cancer Prev Res 2011;4:744-51.
74. Tang JY, Wu A, Linos E, Parimi N, Lee W, Aszterbaum M, et al. High prevalence of vitamin D deficiency in patients with basal cell nevus syndrome. Arch Dermatol 2010;146:1105-10.
75. Tang JY, Chiou AS, Mackay-Wiggan JM, Aszterbaum M, Chanana AM, Lee W, et al. Tazarotene: randomized, double blind, vehicle-controlled and open-label concurrent trials for basal cell carcinoma prevention and therapy in patients with basal cell nevus syndrome. Cancer Prev Res 2014;7:292-9.
76. +/- humans and mice. Cancer Prev Res 2010;3:25-34.
77. Tabs S, Avci O. Induction of the differentiation and apoptosis of tumor cells in vivo with efficiency and selectivity. Eur J Dermatol 2004;14:96-102.
78. Tang T, Tang JY, Li D, Reich M, Callahan CA, Fu L, et al. Targeting superficial or nodular Basal cell carcinoma with topically formulated small molecule inhibitor of smoothened. Clin Cancer Res 2011;17:3378-87.
79. Skvara H, Kalthoff F, Meingassner JG, Wolff-Winiski B, Aschauer H, Kelleher JF, et al. Topical treatment of Basal cell carcinomas in nevoid Basal cell carcinoma syndrome with a smoothened inhibitor. J Invest Dermatol 2011;131:1735-44.
80. Von Hoff DD, Lo Russo PM, Rudin CM, Reddy JC, Yauch RL, Tibes R, et al. Inhibition of the hedgehog pathway in advanced basal-cel carcinoma. N Engl J Med 2009;361:1164-72.
81. Lo Russo PM, Rudin CM, Reddy JC, Tibes R, Weiss GJ, Borad MJ, et al. Phase I trial of hedgehog pathway inhibitor vismodegib (GDC-0449) in patients with refractory, locally advanced or metastatic solid tumors. Clin Cancer Res 2011;17:2502-11.
82. Sharma MR, Karrison TG, Kell B, Wu K, Turcich M, Geary D, et al. Evaluation of food effect on pharmacokinetics of vismodegib in advanced solid tumor patients. Clin Cancer Res 2013;19:3059-67.
83. Tang JY, Mackay-Wiggan JM, Aszterbaum M, Yauch RL, Lindgren J, Chang K, et al. Inhibiting the hedgehog pathway in patients with the basal-cell nevus syndrome. N Engl J Med 2012;366:2180-8.
84. Sekulic A, Migden MR, Oro AE, Dirix L, Lewis KD, Hainsworth JD, et al. Efficacy and safety of vismodegib in advanced basal-cell carcinoma. N Engl J Med 2012;366:2171-9.
85. Axelson M, Liu K, Jiang X, He K, Wang J, Zhao H, et al. U. S. Food and Drug Administration approval: vismodegib for recurrent, locally advanced, or metastatic basal cell carcinoma. Clin Cancer Res 2013;19:2289-93.
86. Aasi S, Silkiss R, Tang JY, Wysong A, Liu A, Epstein E, et al. New onset of keratoacanthomas after vismodegib treatment for locally advanced basal cell carcinomas: a report of 2 cases. JAMA Dermatol 2013;149:242-3.
87. Gill HS, Moscato EE, Chang AL, Soon S, Silkiss RZ. Vismodegib for periocular and orbital Basal cell carcinoma. JAMA Ophthalmol 2013;131:1591-4.
88. Yauch RL, Dijkgraaf GJ, Alicke B, Januario T, Ahn CP, Holcomb T, et al. Smoothened mutation confers resistance to a Hedgehog pathway inhibitor in medulloblastoma. Science 2009;326:572-4.
89. Engelman JA, Settleman J. Acquired resistance to tyrosine kinase inhibitors during cancer therapy. Curr Opin Genet Dev 2008;18:73-9.
90. Tao H, Jin Q, Koo DI, Liao X, Englund NP, Wang Y, et al. Small molecule antagonists in distinct binding modes inhibit drug-resistant mutant of smoothened. Chem Biol 2011;18:432-7.