Detection of primary cilia in human glioblastoma

Journal of Neuro-Oncology

Volumn 117, Issue 1, 2014, Pages 15-24

  Sarkisian, Matthew R ^a   Siebzehnrubl, Dorit ^a   Hoang Minh, Lan ^a   Deleyrolle, Loic ^a   Silver, Daniel J ^a   Siebzehnrubl, Florian A ^a   Guadiana, Sarah M ^a   Srivinasan, Gayathri ^a   Semple Rowland, Susan ^a   Harrison, Jeffrey K ^a   Steindler, Dennis A ^a   Reynolds, Brent A ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Cancer; Cilium; Glioma; Intraflagellar transport

Indexed keywords

ALPHA TUBULIN; ARL13B PROTEIN; CARRIER PROTEIN; GAMMA TUBULIN; GUANOSINE TRIPHOSPHATASE; IFT88 PROTEIN; KI 67 ANTIGEN; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; AXONEME; CELL SURFACE; CILIATED EPITHELIUM; CONTROLLED STUDY; ELECTRON MICROSCOPY; EUKARYOTIC FLAGELLUM; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MICROTUBULE; MIDDLE AGED; TUMOR BIOPSY; VERY ELDERLY;

ADP-RIBOSYLATION FACTORS; AGED, 80 AND OVER; AXONEME; BASAL BODIES; BRAIN NEOPLASMS; CELL LINE, TUMOR; CILIA; GLIOBLASTOMA; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; MALE; MICROSCOPY, ELECTRON; MIDDLE AGED; TRANSCRIPTION FACTORS; TUBULIN; TUMOR SUPPRESSOR PROTEINS;

EID: 84901634102     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-013-1340-y     Document Type: Article

References (43)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996
2. Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H (2012) The brain tumor microenvironment. Glia 60:502-514
3. Hjelmeland AB, Lathia JD, Sathornsumetee S, Rich JN (2011) Twisted tango: brain tumor neurovascular interactions. Nat Neurosci 14:1375-1381
4. Siebzehnrubl FA, Reynolds BA, Vescovi A, Steindler DA, Deleyrolle LP (2011) The origins of glioma: E Pluribus Unum? Glia 59:1135-1147
5. Breunig JJ, Sarkisian MR, Arellano JI, Morozov YM, Ayoub AE, Sojitra S, Wang B, Flavell RA, Rakic P, Town T (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci USA 105:13127-13132
6. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11:277-284
7. Baudoin JP, Viou L, Launay PS, Luccardini C, Espeso Gil S, Kiyasova V, Irinopoulou T, Alvarez C, Rio JP, Boudier T, Lechaire JP, Kessaris N, Spassky N, Metin C (2012) Tangentially migrating neurons assemble a primary cilium that promotes their reorientation to the cortical plate. Neuron 76:1108-1122
8. Higginbotham H, Eom TY, Mariani LE, Bachleda A, Hirt J, Gukassyan V, Cusack CL, Lai C, Caspary T, Anton ES (2012) Arl13b in primary cilia regulates the migration and placement of interneurons in the developing cerebral cortex. Dev Cell 23:925-938
9. Yoshimura K, Kawate T, Takeda S (2011) Signaling through the primary cilium affects glial cell survival under a stressed environment. Glia 59:333-344
10. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, Anderson KV (2003) Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426:83-87
11. Rohatgi R, Milenkovic L, Scott MP (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science 317:372-376
12. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K (2008) Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc Natl Acad Sci USA 105:4242-4246
13. Chakravarthy B, Gaudet C, Menard M, Atkinson T, Chiarini A, Dal Pra I, Whitfield J (2010) The p75 neurotrophin receptor is localized to primary cilia in adult murine hippocampal dentate gyrus granule cells. Biochem Biophys Res Commun 401:458-462
14. Schneider L, Clement CA, Teilmann SC, Pazour GJ, Hoffmann EK, Satir P, Christensen ST (2005) PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr Biol 15:1861-1866
15. Ponten J, Macintyre EH (1968) Long term culture of normal and neoplastic human glia. Acta Pathol Microbiol Scand 74:465-486
16. Stein GH (1979) T98G: an anchorage-independent human tumor cell line that exhibits stationary phase G1 arrest in vitro. J Cell Physiol 99:43-54
17. Moser JJ, Fritzler MJ, Rattner JB (2009) Primary ciliogenesis defects are associated with human astrocytoma/glioblastoma cells. BMC Cancer 9:448
18. Barakat MT, Humke EW, Scott MP (2013) Kif3a is necessary for initiation and maintenance of medulloblastoma. Carcinogenesis 34:1382-1392
19. Han YG, Kim HJ, Dlugosz AA, Ellison DW, Gilbertson RJ, Alvarez-Buylla A (2009) Dual and opposing roles of primary cilia in medulloblastoma development. Nat Med 15:1062-1065
20. Wong SY, Seol AD, So PL, Ermilov AN, Bichakjian CK, Epstein EH Jr, Dlugosz AA, Reiter JF (2009) Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat Med 15:1055-1061
21. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97-109
22. Deleyrolle LP, Harding A, Cato K, Siebzehnrubl FA, Rahman M, Azari H, Olson S, Gabrielli B, Osborne G, Vescovi A, Reynolds BA (2011) Evidence for label-retaining tumour-initiating cells in human glioblastoma. Brain 134:1331-1343
23. Hothi P, Martins TJ, Chen L, Deleyrolle L, Yoon JG, Reynolds B, Foltz G (2012) High-throughput chemical screens identify disulfiram as an inhibitor of human glioblastoma stem cells. Oncotarget 3:1124-1136
24. Aldaz H, Rice LM, Stearns T, Agard DA (2005) Insights into microtubule nucleation from the crystal structure of human gamma-tubulin. Nature 435:523-527
25. Kim J, Lee JE, Heynen-Genel S, Suyama E, Ono K, Lee K, Ideker T, Aza-Blanc P, Gleeson JG (2010) Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464:1048-1051
26. Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL (1993) A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90:5519-5523
27. Ishikawa H, Marshall WF (2011) Ciliogenesis: building the cell's antenna. Nature Rev Mol Cell Biol 12:222-234
28. Santos N, Reiter JF (2008) Building it up and taking it down: the regulation of vertebrate ciliogenesis. Dev Dyn 237:1972-1981
29. Caspary T, Larkins CE, Anderson KV (2007) The graded response to Sonic Hedgehog depends on cilia architecture. Dev Cell 12:767-778
30. Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182:311-322
31. Siebzehnrubl FA, Silver DJ, Tugertimur B, Deleyrolle LP, Siebzehnrubl D, Sarkisian MR, Devers KG, Yachnis AT, Kupper MD, Neal D, Nabilsi NH, Kladde MP, Suslov O, Brabletz S, Brabletz T, Reynolds BA, Steindler DA (2013) The ZEB1 pathway links glioblastoma initiation, invasion and chemoresistance. EMBO Mol Med 5:1196-1212
32. Basten SG, Willekers S, Vermaat JS, Slaats GG, Voest EE, van Diest PJ, Giles RH (2013) Reduced cilia frequencies in human renal cell carcinomas versus neighboring parenchymal tissue. Cilia 2:2
33. Kim J, Dabiri S, Seeley ES (2011) Primary cilium depletion typifies cutaneous melanoma in situ and malignant melanoma. PLoS One 6:e27410
34. Seeley ES, Carriere C, Goetze T, Longnecker DS, Korc M (2009) Pancreatic cancer and precursor pancreatic intraepithelial neoplasia lesions are devoid of primary cilia. Cancer Res 69:422-430
35. van Asselt SJ, de Vries EG, van Dullemen HM, Brouwers AH, Walenkamp AM, Giles RH, Links TP (2013) Pancreatic cyst development: insights from von Hippel-Lindau disease. Cilia 2:3
36. Yuan K, Frolova N, Xie Y, Wang D, Cook L, Kwon YJ, Steg AD, Serra R, Frost AR (2010) Primary cilia are decreased in breast cancer: analysis of a collection of human breast cancer cell lines and tissues. J Histochem Cytochem 58:857-870
37. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9:391-403
38. Leask A, Obrietan K, Stearns T (1997) Synaptically coupled central nervous system neurons lack centrosomal gamma-tubulin. Neurosci Lett 229:17-20
39. O'Connor AK, Malarkey EB, Berbari NF, Croyle MJ, Haycraft CJ, Bell PD, Hohenstein P, Kesterson RA, Yoder BK (2013) An inducible CiliaGFP mouse model for in vivo visualization and analysis of cilia in live tissue. Cilia 2:8
40. Fukushima N, Furuta D, Hidaka Y, Moriyama R, Tsujiuchi T (2009) Post-translational modifications of tubulin in the nervous system. J Neurochem 109:683-693
41. Plotnikova OV, Golemis EA, Pugacheva EN (2008) Cell cycle-dependent ciliogenesis and cancer. Cancer Res 68:2058-2061
42. Yang Y, Roine N, Makela TP (2013) CCRK depletion inhibits glioblastoma cell proliferation in a cilium-dependent manner. EMBO Rep 14:741-747
43. Silver DJ, Siebzehnrubl FA, Schildts MJ, Yachnis AT, Smith GM, Smith AA, Scheffler B, Reynolds BA, Silver J, Steindler DA (2013) Chondroitin sulfate proteoglycans potently inhibit invasion and serve as a central organizer of the brain tumor microenvironment. J Neurosci 33:15603-15617