Molecular pathways: The role of primary cilia in cancer progression and therapeutics with a focus on hedgehog signaling

Clinical Cancer Research

Volumn 18, Issue 9, 2012, Pages 2429-2435

  Hassounah, Nadia B ^a   Bunch, Thomas A ^b   McDermott, Kimberly M ^a,b,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; GANT 61; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; UNCLASSIFIED DRUG; VISMODEGIB;

ARTICLE; CANCER CELL; CANCER GROWTH; CANCER THERAPY; CARCINOGENESIS; CELL FUNCTION; CELL INTERACTION; CELL ORGANELLE; CELL PROLIFERATION; DISEASE ASSOCIATION; DRUG MECHANISM; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIMARY CILIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CILIA; HEDGEHOG PROTEINS; HUMANS; NEOPLASMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

EID: 84860536549     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-0755     Document Type: Article

References (47)

1. Ostrowski LE, Blackburn K, Radde KM, Moyer MB, Schlatzer DM, Moseley A, et al. A proteomic analysis of human cilia: identification of novel components. Mol Cell Proteomics 2002;1:451-65.
2. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 2004;117:541-52. (Pubitemid 38610238)
3. Smith JC, Northey JG, Garg J, Pearlman RE, Siu KW. Robust method for proteome analysis by MS/MS using an entire translated genome: demonstration on the ciliome of Tetrahymena thermophila. J Proteome Res 2005;4:909-19. (Pubitemid 40863280)
4. Pazour GJ, Agrin N, Leszyk J, Witman GB. Proteomic analysis of a eukaryotic cilium. J Cell Biol 2005;170:103-13. (Pubitemid 40994100)
5. Gherman A, Davis EE, Katsanis N. The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat Genet 2006;38:961-2. (Pubitemid 44325911)
6. Inglis PN, Boroevich KA, Leroux MR. Piecing together a ciliome. Trends Genet 2006;22:491-500. (Pubitemid 44233721)
7. Wagner V, Gessner G, Heiland I, Kaminski M, Hawat S, Scheffler K, et al. Analysis of the phosphoproteome of Chlamydomonas reinhardtii provides new insights into various cellular pathways. Eukaryot Cell 2006;5:457-68.
8. Liu Q, Tan G, Levenkova N, Li T, Pugh EN Jr, Rux JJ, et al. The proteome of the mouse photoreceptor sensory cilium complex. Mol Cell Proteomics 2007;6:1299-317. (Pubitemid 47365430)
9. Mayer U, Küller A, Daiber PC, Neudorf I, Warnken U, Schnölzer M, et al. The proteome of rat olfactory sensory cilia. Proteomics 2009;9:322-34.
10. Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol 2002;3:813-25. (Pubitemid 35285272)
11. Scholey JM. Intraflagellar transport. Annu Rev Cell Dev Biol 2003;19:423-43. (Pubitemid 37487355)
12. Pazour GJ. Intraflagellar transport and cilia-dependent renal disease: the ciliary hypothesis of polycystic kidney disease. J Am Soc Nephrol 2004;15:2528-36. (Pubitemid 41103359)
13. Ware SM, Aygun MG, Hildebrandt F. Spectrum of clinical diseases caused by disorders of primary cilia. Proc Am Thorac Soc 2011;8:444-50.
14. Corbit KC, Aanstad P, Singla V, Norman AR, Stainier DY, Reiter JF. Vertebrate Smoothened functions at the primary cilium. Nature 2005;437:1018-21. (Pubitemid 41486982)
15. Haycraft CJ, Banizs B, Aydin-Son Y, Zhang Q, Michaud EJ, Yoder BK. Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet 2005;1:e53.
16. Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, Krönig C, et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 2005;37:537-43. (Pubitemid 40617284)
17. Schneider L, Clement CA, Teilmann SC, Pazour GJ, Hoffmann EK, Satir P, et al. PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr Biol 2005;15:1861-6. (Pubitemid 41501522)
18. Corbit KC, Shyer AE, Dowdle WE, Gaulden J, Singla V, Chen MH, et al. Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat Cell Biol 2008;10:70-6.
19. Lancaster MA, Schroth J, Gleeson JG. Subcellular spatial regulation of canonical Wnt signalling at the primary cilium. Nat Cell Biol 2011;13: 700-7.
20. Goetz SC, Anderson KV. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 2010;11:331-44.
21. Hu Q, Milenkovic L, Jin H, Scott MP, Nachury MV, Spiliotis ET, et al. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 2010;329:436-9.
22. Nachury MV, Seeley ES, Jin H. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol 2010;26:59-87.
23. Rohatgi R, Milenkovic L, Scott MP. Patched1 regulates hedgehog signaling at the primary cilium. Science 2007;317:372-6. (Pubitemid 47106377)
24. Humke EW, Dorn KV, Milenkovic L, Scott MP, Rohatgi R. The output of Hedgehog signaling is controlled by the dynamic association between Suppressor of Fused and the Gli proteins. Genes Dev 2010;24:670-82.
25. Milenkovic L, Scott MP, Rohatgi R. Lateral transport of Smoothened from the plasma membrane to the membrane of the cilium. J Cell Biol 2009;187:365-74.
26. Chen Y, Sasai N, Ma G, Yue T, Jia J, Briscoe J, et al. Sonic Hedgehog dependent phosphorylation by CK1a and GRK2 is required for ciliary accumulation and activation of smoothened. PLoS Biol 2011;9:e1001083.
27. Tukachinsky H, Lopez LV, Salic A. A mechanism for vertebrate Hedgehog signaling: recruitment to cilia and dissociation of SuFu-Gli protein complexes. J Cell Biol 2010;191:415-28.
28. Teglund S, Toftgard R. Hedgehog beyond medulloblastoma and basal cell carcinoma. Biochim Biophys Acta 2010;1805:181-208.
29. Wong SY, Seol AD, So PL, Ermilov AN, Bichakjian CK, Epstein EH Jr, et al. Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat Med 2009;15:1055-61.
30. Han YG, Kim HJ, Dlugosz AA, Ellison DW, Gilbertson RJ, Alvarez- Buylla A. Dual and opposing roles of primary cilia in medulloblastoma development. Nat Med 2009;15:1062-5.
31. Schraml P, Frew IJ, Thoma CR, Boysen G, Struckmann K, Krek W, et al. Sporadic clear cell renal cell carcinoma but not the papillary type is characterized by severely reduced frequency of primary cilia. Mod Pathol 2009;22:31-6.
32. Yuan K, Frolova N, Xie Y, Wang D, Cook L, Kwon YJ, et al. Primary cilia are decreased in breast cancer: analysis of a collection of human breast cancer cell lines and tissues. J Histochem Cytochem 2010;58:857-70.
33. Seeley ES, Carrière C, Goetze T, Longnecker DS, Korc M. Pancreatic cancer and precursor pancreatic intraepithelial neoplasia lesions are devoid of primary cilia. Cancer Res 2009;69:422-30.
34. Kim J, Dabiri S, Seeley ES. Primary ciliumdepletion typifies cutaneous melanoma in situ and malignant melanoma. PLoS ONE 2011;6:e27410.
35. Chai H, Brown RE. Field effect in cancer-an update. Ann Clin Lab Sci 2009;39:331-7.
36. Ng JM, Curran T. The Hedgehog's tale: developing strategies for targeting cancer. Nat Rev Cancer 2011;11:493-501.
37. Scales SJ, de Sauvage FJ. Mechanisms of Hedgehog pathway activation in cancer and implications for therapy. Trends Pharmacol Sci 2009;30:303-12.
38. Gupta S, Takebe N, Lorusso P. Targeting the Hedgehog pathway in cancer. Ther Adv Med Oncol 2010;2:237-50.
39. Merchant AA, Matsui W. Targeting Hedgehog - a cancer stem cell pathway. Clin Cancer Res 2010;16:3130-40.
40. Hyman JM, Firestone AJ, Heine VM, Zhao Y, Ocasio CA, Han K, et al. Small-molecule inhibitors reveal multiple strategies for Hedgehog pathway blockade. Proc Natl Acad Sci U S A 2009;106:14132-7.
41. Kasper M, Regl G, Frischauf AM, Aberger F. GLI transcription factors: mediators of oncogenic Hedgehog signalling. Eur J Cancer 2006;42:437-45. (Pubitemid 43227920)
42. Sheng T, Li C, Zhang X, Chi S, He N, Chen K, et al. Activation of the hedgehog pathway in advanced prostate cancer. Mol Cancer 2004;3:29.
43. Tostar U, Malm CJ, Meis-Kindblom JM, Kindblom LG, Toftgård R, Undén AB. Deregulation of the hedgehog signalling pathway: a possible role for the PTCH and SUFU genes in human rhabdomyoma and rhabdomyosarcoma development. J Pathol 2006;208:17-25. (Pubitemid 43025700)
44. Di Marcotullio L, Ferretti E, De Smaele E, Argenti B, Mincione C, Zazzeroni F, et al. REN(KCTD11) is a suppressor of Hedgehog signaling and is deleted in human medulloblastoma. Proc Natl Acad Sci U S A 2004;101:10833-8. (Pubitemid 38955828)
45. Cervantes S, Lau J, Cano DA, Borromeo-Austin C, Hebrok M. Primary cilia regulate Gli/Hedgehog activation in pancreas. Proc Natl Acad Sci U S A 2010;107:10109-14.
46. Lauth M, Bergström A, Shimokawa T, Toftgård R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci U S A 2007;104:8455-60. (Pubitemid 47175509)
47. Von Hoff DD, LoRusso PM, Rudin CM, Reddy JC, Yauch RL, Tibes R, et al. Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. N Engl J Med 2009;361:1164-72.