The Activation of the WNT signaling pathway is a hallmark in neurofibromatosis type 1 tumorigenesis

Clinical Cancer Research

Volumn 20, Issue 2, 2014, Pages 358-371

  Luscan, Armelle ^a,c   Shackleford, Ghjuvan Ghjacumu ^d   Masliah Planchon, Julien ^a   Laurendeau, Ingrid ^a   Ortonne, Nicolas ^c   Varin, Jennifer ^a   Lallemand, Fraņcois ^a,c   Leroy, Karen ⁱ   Dumaine, Valérie ^e   Hivelin, Mikael ^b,c   Borderie, Didier ^f   De Raedt, Thomas ^l   Valeyrie Allanore, Laurence ^j   Larousserie, Frédeérique ^g   Terris, Benoît ^c,h   Lantieri, Laurent ^b   Vidaud, Michel ^a,c   Vidaud, Dominique ^a,c   Wolkenstein, Pierre ^j   Parfait, Béatrice ^a,c   Bièche, Ivan ^a,k   Massaad, Charbel ^d   Pasmant, Eric ^a,c   more..

^a INSERM   (France)

^b HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^d Paris Descartes   (France)

^e Department of Orthopedic Surgery   (India)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g Paris Descartes University ^*  (France)

^h CNRS   (France)

ⁱ Université Paris Est Créteil ^*  (France)

^j HENRI MONDOR HOSPITAL   (France)

^k INSTITUT CURIE   (France)

^l BRIGHAM AND WOMEN S HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; WNT PROTEIN;

ARTICLE; CARCINOGENESIS; CDH1 GENE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; MALIGNANT PERIPHERAL NERVE SHEATH TUMOR; MARKER GENE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NEUROFIBROMATOSIS; NKX2.2 GENE; ONCOGENE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROM1 GENE; PROTEIN DETERMINATION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SCREENING TEST; SIGNAL TRANSDUCTION; SLUG GENE; SMT GENE; SNAIL GENE; STEMNESS GENE; TWIST1 GENE; VIM GENE; WNT GENE;

BIOLOGICAL MARKERS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; ENDOTHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOPHENOTYPING; MAST CELLS; NEUROFIBROMA; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SCHWANN CELLS; STEM CELLS; WNT SIGNALING PATHWAY;

EID: 84892744573     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-0780     Document Type: Article

References (52)

1. Friedman JM. Epidemiology of neurofibromatosis type 1. Am J Med Genet 1999;89:1-6.
2. Sabbagh A, Pasmant E, Laurendeau I, Parfait B, Barbarot S, Guillot B, et al. Unravelling the genetic basis of variable clinical expression in neurofibromatosis 1. Hum Mol Genet 2009;18:2768-78.
3. Zhu Y, Ghosh P, Charnay P, Burns DK, Parada LF. Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science 2002;296:920-2.
4. Zheng H, Chang L, Patel N, Yang J, Lowe L, Burns DK, et al. Induction of abnormal proliferation by nonmyelinating schwann cells triggers neurofibroma formation. Cancer Cell 2008;13: 117-28.
5. Le LQ, Shipman T, Burns DK, Parada LF. Cell of origin and microenvironment contribution for NF1-associated dermal neurofibromas. Cell Stem Cell 2009;4:453-63.
6. Leroy K, Dumas V, Martin-Garcia N, Falzone MC, Voisin MC, Wechsler J, et al. Malignant peripheral nerve sheath tumors associated with neurofibromatosis type 1: A clinicopathologic and molecular study of 17 patients. Arch Dermatol 2001;137:908-13.
7. Tucker T, Wolkenstein P, Revuz J, Zeller J, Friedman JM. Association between benign and malignant peripheral nerve sheath tumors in NF1. Neurology 2005;65:205-11.
8. Menon AG, Anderson KM, Riccardi VM, Chung RY, Whaley JM, Yandell DW, et al. Chromosome17p deletions and p53 gene mutations associated with the formation of malignant neurofibrosarcomas in von Recklinghausen neurofibromatosis. Proc Natl Acad Sci US A 1990;87: 5435-9.
9. Kourea HP, Cordon-Cardo C, Dudas M, Leung D, Woodruff JM. Expression of p27(kip) and other cell cycle regulators in malignant peripheral nerve sheath tumors and neurofibromas: The emerging role of p27(kip) in malignant transformation of neurofibromas. Am J Pathol 1999;155:1885-91.
10. Nielsen GP, Stemmer-Rachamimov AO, Ino Y, Moller MB, Rosenberg AE, Louis DN. Malignant transformation of neurofibromas in neurofibromatosis 1 is associated with CDKN2A/p16 inactivation. Am J Pathol 1999;155:1879-84.
11. DeClue JE, Heffelfinger S, Benvenuto G, Ling B, Li S, Rui W, et al. Epidermal growth factor receptor expression in neurofibromatosis type 1-related tumors and NF1 animal models. J Clin Invest 2000;105: 1233-41.
12. Perrone F, Tabano S, Colombo F, Dagrada G, Birindelli S, Gronchi A, et al. p15INK4b, p14ARF, and p16INK4a inactivation in sporadic and neurofibromatosis type 1-related malignant peripheral nerve sheath tumors. Clin Cancer Res 2003;9:4132-8.
13. Polyak K, Hahn WC. Roots and stems: stem cells in cancer. Nat Med 2006;12:296-300.
14. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005;434:843-50.
15. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-90.
16. Joseph NM, Mosher JT, Buchstaller J, Snider P, McKeever PE, Lim M, et al. The loss of Nf1 transiently promotes self-renewal but not tumorigenesis by neural crest stem cells. Cancer Cell 2008;13: 129-40.
17. Williams JP,WuJ, Johansson G, Rizvi TA, Miller SC, Geiger H, et al. Nf1 mutation expands an EGFR-dependent peripheral nerve progenitor that confers neurofibroma tumorigenic potential. Cell Stem Cell 2008;3:658-69.
18. Lévy P, Vidaud D, Leroy K, Laurendeau I, Wechsler J, Bolasco G, et al. Molecular profiling of malignant peripheral nerve sheath tumors associated with neurofibromatosis type 1, based on large-scale real-time RT-PCR. Mol Cancer 2004;3:20.
19. Miller SJ, Rangwala F, Williams J, Ackerman P, Kong S, Jegga AG, et al. Large-scale molecular comparison of human schwann cells to malignant peripheral nerve sheath tumor cell lines and tissues. Cancer Res 2006;66:2584-91.
20. Angers S, Moon RT. Proximal events in Wnt signal transduction. Not as tenants in common Rev Mol Cell Biol 2009;10:468-77.
21. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008;8:387-98.
22. Takebe N, Harris PJ, Warren RQ, Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol 2011;8:97-106.
23. Avellana-Adalid V, Bachelin C, Lachapelle F, Escriou C, Ratzkin B, Baron-Van Evercooren A. In vitro and in vivo behaviour of NDFexpanded monkey Schwann cells. Eur J Neurosci 1998;10:291-300.
24. Bachelin C, Lachapelle F, Girard C, Moissonnier P, Serguera-Lagache C, Mallet J, et al. Efficient myelin repair in the macaque spinal cord by autologous grafts of Schwann cells. Brain 2005;128:540-9.
25. Rosenbaum T, Rosenbaum C, Winner U, Müller HW, Lenard HG, Hanemann CO. Long-term culture and characterization of human neurofibroma-derived Schwann cells. J Neurosci Res 2000;61: 524-32.
26. Royer B, Varadaradjalou S, Saas P, Gabiot AC, Kantelip B, Féger F, et al. Autocrine regulation of cord blood-derived human mast cell activation by IL-10. J Allergy Clin Immunol 2001;108:80-6.
27. Boutry JM,HauwJJ,Gansmuller A, Di-Bert N, Pouchelet M, Baron-Van Evercooren A. Establishment and characterization of a mouse Schwann cell line which produces myelin in vivo. J Neurosci Res 1992;32:15-26.
28. Pasmant E, Masliah-Planchon J, Lévy P, Laurendeau I, Ortonne N, Parfait B, et al. Identification of genes potentially involved in the increased risk of malignancy in NF1-microdeleted patients. Mol Med 2011;17:79-87.
29. Pasmant E, Ortonne N, Rittié L, Laurendeau I, Lévy P, Lazar V, et al. Differential expression of CCN1/CYR61, CCN3/NOV, CCN4/WISP1, and CCN5/WISP2 in neurofibromatosis type 1 tumorigenesis. J Neuropathol Exp Neurol 2010;69:60-9.
30. Massaad C, Garlatti M, Wilson EM, Cadepond F, Barouki R. A natural sequence consisting of overlapping glucocorticoid-responsive elements mediates glucocorticoid, but not androgen, regulation of gene expression. Biochem J 2000;1:123-9.
31. Behrens J, Lustig B. The Wnt connection to tumorigenesis. Int J Dev Biol 2004;48:477-87.
32. Matushansky I, Hernando E, Socci ND, Mills JE, Matos TA, Edgar MA, et al. Derivation of sarcomas from mesenchymal stem cells via inactivation of the Wnt pathway. J Clin Invest 2007;117:3248-57.
33. Brohlin M, Mahay D, Novikov LN, Terenghi G, Wiberg M, Shawcross SG, et al. Characterisation of human mesenchymal stem cells following differentiation into Schwann cell-like cells. Neurosci Res 2009;64: 41-9.
34. Tawk M, Makoukji J, Belle M, Fonte C, Trousson A, Hawkins T, et al. Wnt/β-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J Neurosci 2011;31:3729-42.
35. Makoukji J, Belle M, Meffre D, Stassart R, Grenier J, Shackleford G, et al. Lithium enhances remyelination of peripheral nerves. Proc Natl Acad Sci U S A 2012;109:3973-8.
36. Flahaut M, Meier R, Coulon A, Nardou KA, Niggli FK, Martinet D, et al. The Wnt receptor FZD1 mediates chemoresistance in neuroblastoma through activation of the Wnt/β-catenin pathway. Oncogene 2009;28: 2245-56.
37. Tang D, Liu J, Wang DR, Yu HF, Li YK, Zhang JQ. Diagnostic and prognostic value of the methylation status of secreted frizzled-related protein 2 in colorectal cancer. Clin Invest Med 2011;34:E88-95.
38. Cowling VH, D'Cruz CM, Chodosh LA, Cole MD. c-Myc transforms human mammary epithelial cells through repression of the Wnt inhibitors DKK1 and SFRP1. Mol Cell Biol 2007;27:5135-46.
39. Rorive S, Maris C, Debeir O, Sandras F, Vidaud M, Biéche I, et al. Exploring the distinctive biological characteristics of pilocytic and lowgrade diffuse astrocytomas using microarray gene expression profiles. J Neuropathol Exp Neurol 2006;65:794-807.
40. Kuphal S, Lodermeyer S, Bataille F, Schuierer M, Hoang BH, Bosserhoff AK. Expression of Dickkopf genes is strongly reduced in malignant melanoma. Oncogene 2006;25:5027-36.
41. Miller SJ, Jessen WJ, Mehta T, Hardiman A, Sites E, Kaiser S, et al. Integrative genomic analyses of neurofibromatosis tumours identify SOX9 as a biomarker and survival gene. EMBO Mol Med 2009;1: 236-48.
42. Endo M, Yamamoto H, Setsu N, Kohashi K, Takahashi Y, Ishii T, et al. Prognostic significance of AKT/mTOR and MAPK pathways and antitumor effect of mTOR inhibitor in NF1-related and sporadic malignant peripheral nerve sheath tumors. Clin Cancer Res 2013;19: 450-61.
43. Dissanayake SK, Olkhanud PB, O'Connell MP, Carter A, French AD, Camilli TC, et al. Wnt5A regulates expression of tumor-associated antigens in melanomavia changes in signal transducers and activators of transcription 3 phosphorylation. Cancer Res 2008;68:10205-14.
44. Danilkovitch-Miagkova A, Miagkov A, Skeel A, Nakaigawa N, Zbar B, Leonard EJ. Oncogenic mutants of RON and MET receptor tyrosine kinases cause activation of the β-catenin pathway. Mol Cell Biol 2001;21:5857-68.
45. Bonvini P, An WG, Rosolen A, Nguyen P, Trepel J, Garcia de Herreros A, et al. Geldanamycin abrogates ErbB2 association with proteasomeresistant β-catenin in melanoma cells, increases β-catenin-E-cadherin association, and decreases β-catenin-sensitive transcription. Cancer Res 2001;61:1671-7.
46. Zhou L, An N, Haydon RC, Zhou Q, Cheng H, Peng Y, et al. Tyrosine kinase inhibitor STI-571/Gleevec down-regulates the β-catenin signaling activity. Cancer Lett 2003;193:161-70.
47. Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K, et al. Atwo-step model for colon adenoma initiation and progression caused by APC loss. Cell 2009;137:623-34.
48. Pearson HB, Phesse TJ, Clarke AR. K-ras and Wnt signaling synergize to accelerate prostate tumorigenesis in the mouse. Cancer Res 2009;69:94-101.
49. Nteliopoulos G, Marley SB, Gordon MY. Influence of PI-3K/Akt pathway on Wnt signalling in regulating myeloid progenitor cell proliferation. Evidence for a role of autocrine/paracrine Wnt regulation. Br J Haematol 2009;146:637-51.
50. Howe LR, Watanabe O, Leonard J, Brown AM. Twist is up-regulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res 2003;63:1906-13.
51. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 2007;17:165-72.
52. Stevenson DA, Zhou H, Ashrafi S, Messiaen LM, Carey JC, D'Astous JL, et al. Double inactivation of NF1 in tibial pseudarthrosis. Am J Hum Genet 2006;79:143-8.