Wild-type ALK and activating ALK-R1275Q and ALK-F1174L mutations upregulate Myc and initiate tumor formation in murine neural crest progenitor cells

Oncotarget

Volumn 5, Issue 12, 2014, Pages 4452-4466

  Montavon, Gisèle ^a   Jauquier, Nicolas ^b   Coulon, Aurélie ^b   Peuchmaur, Michel ^c   Flahaut, Marjorie ^b   Bourloud, Katia Balmas ^b   Yan, Pu ^b   Delattre, Olivier ^d   Sommer, Lukas ^e   Joseph, Jean Marc ^b   Janoueix Lerosey, Isabelle ^d   Gross, Nicole ^b   Mühlethaler Mottet, Annick ^b  

^a Pediatric Department HFR Hospital Fribourg   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c HÔPITAL ROBERT DEBRÉ   (France)

^d INSTITUT CURIE   (France)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

ALK; Myc; Neuroblastoma; Sifferentiation; Tumorigenesis

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; MYC PROTEIN; TAMOXIFEN; PROTEIN TYROSINE KINASE;

ALK F1174L GENE; ALK R1275Q GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CHONDROSARCOMA; CONTROLLED STUDY; FEMALE; GAIN OF FUNCTION MUTATION; GENE ACTIVATION; GENE ACTIVITY; GENE FUNCTION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC STABILITY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; JOMA1 CELL LINE; MONC 1 CELL LINE; MOUSE; NEURAL CREST CELL; NEURAL STEM CELL; NEUROBLASTOMA; NONHUMAN; ONCOGENE MYC; OSTEOSARCOMA; TUMOR CELL INOCULATION; TUMOR CELL LINE; TUMOR DIFFERENTIATION; UNDIFFERENTIATED CARCINOMA; UPREGULATION; WILD TYPE; ANIMAL; GENETICS; METABOLISM; MUTATION; NEURAL CREST; PHOSPHORYLATION; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; GENES, MYC; HUMANS; MICE; MUTATION; NEURAL CREST; NEUROBLASTOMA; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; STEM CELLS; UP-REGULATION;

EID: 84905086382     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2036     Document Type: Article

References (52)

1. Cheung NK and Dyer MA. Neuroblastoma: developmental biology, cancer genomics and immunotherapy. Nat Rev Cancer. 2013; 13(6):397-411.
2. Le Douarin NM, Calloni GW and Dupin E. The stem cells of the neural crest. Cell Cycle. 2008; 7(8):1013-1019.
3. Le Douarin NM, Creuzet S, Couly G and Dupin E. Neural crest cell plasticity and its limits. Development. 2004; 131(19):4637-4650.
4. Jiang M, Stanke J and Lahti JM. The connections between neural crest development and neuroblastoma. Current topics in developmental biology. 2011; 94:77-127.
5. Azarova AM, Gautam G and George RE. Emerging importance of ALK in neuroblastoma. Semin Cancer Biol. 2011; 21(4):267-275.
6. ReiffT, Huber L, Kramer M, Delattre O, Janoueix-Lerosey I and Rohrer H. Midkine and Alk signaling in sympathetic neuron proliferation and neuroblastoma predisposition. Development. 2011; 138(21):4699-4708.
7. Hallberg B and Palmer RH. Mechanistic insight into ALK receptor tyrosine kinase in human cancer biology. Nat Rev Cancer. 2013; 13(10):685-700.
8. Cheng LY, Bailey AP, Leevers SJ, Ragan TJ, Driscoll PC and Gould AP. Anaplastic lymphoma kinase spares organ growth during nutrient restriction in Drosophila. Cell. 2011; 146(3):435-447.
9. Yao S, Cheng M, Zhang Q, Wasik M, Kelsh R and Winkler C. Anaplastic lymphoma kinase is required for neurogenesis in the developing central nervous system of zebrafish. PLoS ONE. 2013; 8(5):e63757.
10. De Brouwer S, De Preter K, Kumps C, Zabrocki P, Porcu M, Westerhout EM, Lakeman A, Vandesompele J, Hoebeeck J, Van Maerken T, De Paepe A, Laureys G, Schulte JH, Schramm A, Van Den Broecke C, Vermeulen J, et al. Meta-analysis of neuroblastomas reveals a skewed ALK mutation spectrum in tumors with MYCN amplification. Clin Cancer Res. 2010; 16(17):4353-4362.
11. Pugh TJ, Morozova O, Attiyeh EF, Asgharzadeh S, Wei JS, Auclair D, Carter SL, Cibulskis K, Hanna M, Kiezun A, Kim J, Lawrence MS, Lichenstein L, McKenna A, Pedamallu CS, Ramos AH, et al. The genetic landscape of high-risk neuroblastoma. Nat Genet. 2013; 45(3):279-284.
12. Caren H, Abel F, Kogner P and Martinsson T. High incidence of DNA mutations and gene amplifications of the ALK gene in advanced sporadic neuroblastoma tumours. Biochem J. 2008; 416(2):153-159.
13. Chen Y, Takita J, Choi YL, Kato M, Ohira M, Sanada M, Wang L, Soda M, Kikuchi A, Igarashi T, Nakagawara A, Hayashi Y, Mano H and Ogawa S. Oncogenic mutations of ALK kinase in neuroblastoma. Nature. 2008; 455(7215):971-974.
14. George RE, Sanda T, Hanna M, Frohling S, Luther W, 2nd, Zhang J, Ahn Y, Zhou W, London WB, McGrady P, Xue L, Zozulya S, Gregor VE, Webb TR, Gray NS, Gilliland DG, et al. Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature. 2008; 455(7215):975-978.
15. Janoueix-Lerosey I, Lequin D, Brugieres L, Ribeiro A, de Pontual L, Combaret V, Raynal V, Puisieux A, Schleiermacher G, Pierron G, Valteau-Couanet D, Frebourg T, Michon J, Lyonnet S, Amiel J and Delattre O. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature. 2008; 455(7215):967-970.
16. Mosse YP, Laudenslager M, Longo L, Cole KA, Wood A, Attiyeh EF, Laquaglia MJ, Sennett R, Lynch JE, Perri P, Laureys G, Speleman F, Kim C, Hou C, Hakonarson H, Torkamani A, et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature. 2008; 455(7215):930-935.
17. Passoni L, Longo L, Collini P, Coluccia AM, Bozzi F, Podda M, Gregorio A, Gambini C, Garaventa A, Pistoia V, Del Grosso F, Tonini GP, Cheng M, Gambacorti-Passerini C, Anichini A, Fossati-Bellani F, et al. Mutation-independent anaplastic lymphoma kinase overexpression in poor prognosis neuroblastoma patients. Cancer Res. 2009; 69(18):7338-7346.
18. Schulte JH, Bachmann HS, Brockmeyer B, Depreter K, Oberthur A, Ackermann S, Kahlert Y, Pajtler K, Theissen J, Westermann F, Vandesompele J, Speleman F, Berthold F, Eggert A, Brors B, Hero B, et al. High ALK receptor tyrosine kinase expression supersedes ALK mutation as a determining factor of an unfavorable phenotype in primary neuroblastoma. Clin Cancer Res. 2011; 17(15):5082-5092.
19. Mano H. ALKoma: A Cancer Subtype with a Shared Target. Cancer discovery. 2012; 2(6):495-502.
20. Schonherr C, Ruuth K, Eriksson T, Yamazaki Y, Ottmann C, Combaret V, Vigny M, Kamaraj S, Palmer RH and Hallberg B. The neuroblastoma ALK(I1250T) mutation is a kinase-dead RTK in vitro and in vivo. Translational oncology. 2011; 4(4):258-265.
21. Schonherr C, Ruuth K, Kamaraj S, Wang CL, Yang HL, Combaret V, Djos A, Martinsson T, Christensen JG, Palmer RH and Hallberg B. Anaplastic Lymphoma Kinase (ALK) regulates initiation of transcription of MYCN in neuroblastoma cells. Oncogene. 2012.
22. Schulte JH, Lindner S, Bohrer A, Maurer J, De Preter K, Lefever S, Heukamp L, Schulte S, Molenaar J, Versteeg R, Thor T, Kunkele A, Vandesompele J, Speleman F, Schorle H, Eggert A, et al. MYCN and ALKF1174L are sufficient to drive neuroblastoma development from neural crest progenitor cells. Oncogene. 2013; 32(8):1059-1065.
23. Heukamp LC, Thor T, Schramm A, De Preter K, Kumps C, De Wilde B, Odersky A, Peifer M, Lindner S, Spruessel A, Pattyn F, Mestdagh P, Menten B, Kuhfittig-Kulle S, Kunkele A, Konig K, et al. Targeted Expression of Mutated ALK Induces Neuroblastoma in Transgenic Mice. Science translational medicine. 2012; 4(141):141ra191.
24. Berry T, Luther W, Bhatnagar N, Jamin Y, Poon E, Sanda T, Pei D, Sharma B, Vetharoy WR, Hallsworth A, Ahmad Z, Barker K, Moreau L, Webber H, Wang W, Liu Q, et al. The ALK(F1174L) mutation potentiates the oncogenic activity of MYCN in neuroblastoma. Cancer Cell. 2012; 22(1):117-130.
25. Zhu S, Lee JS, Guo F, Shin J, Perez-Atayde AR, Kutok JL, Rodig SJ, Neuberg DS, Helman D, Feng H, Stewart RA, Wang W, George RE, Kanki JP and Look AT. Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell. 2012; 21(3):362-373.
26. Cazes A, Lopez-Delisle L, Tsarovina K, Pierre-Eugène C, De Preter K, Peuchmaur M, Nicolas A, Provost C, Louis-Brennetot C, Daveau R, Kumps C, Cascone I, Schleiermacher G, Prignon A, Speleman F, Rohrer H, et al. Activated Alk triggers prolonged neurogenesis and Ret upregulation providing a therapeutic target in ALK-mutated neuroblastoma. Oncotarget. 2014. Apr 2. [Epub ahead of print]
27. Ogawa S, Takita J, Sanada M and Hayashi Y. Oncogenic mutations of ALK in neuroblastoma. Cancer Sci. 2011; 102(2):302-308.
28. Rao MS and Anderson DJ. Immortalization and controlled in vitro differentiation of murine multipotent neural crest stem cells. J Neurobiol. 1997; 32(7):722-746.
29. Maurer J, Fuchs S, Jager R, Kurz B, Sommer L and Schorle H. Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation. 2007; 75(7):580-591.
30. Bielle F, Freneaux P, Jeanne-Pasquier C, Maran-Gonzalez A, Rousseau A, Lamant L, Paris R, Pierron G, Nicolas AV, Sastre-Garau X, Delattre O, Bourdeaut F and Peuchmaur M. PHOX2B immunolabeling: a novel tool for the diagnosis of undifferentiated neuroblastomas among childhood small round blue-cell tumors. The American journal of surgical pathology. 2012; 36(8):1141-1149.
31. Alam G, Cui H, Shi H, Yang L, Ding J, Mao L, Maltese WA and Ding HF. MYCN promotes the expansion of Phox2B-positive neuronal progenitors to drive neuroblastoma development. Am J Pathol. 2009; 175(2):856-866.
32. Hansford LM, Thomas WD, Keating JM, Burkhart CA, Peaston AE, Norris MD, Haber M, Armati PJ, Weiss WA and Marshall GM. Mechanisms of embryonal tumor initiation: distinct roles for MycN expression and MYCN amplification. Proc Natl Acad Sci U S A. 2004; 101(34):12664-12669.
33. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007; 131(5):861-872.
34. Gouzi JY, Moog-Lutz C, Vigny M and Brunet-de Carvalho N. Role of the subcellular localization of ALK tyrosine kinase domain in neuronal differentiation of PC12 cells. J Cell Sci. 2005; 118(Pt 24):5811-5823.
35. Duijkers FA, Gaal J, Meijerink JP, Admiraal P, Pieters R, de Krijger RR and van Noesel MM. High anaplastic lymphoma kinase immunohistochemical staining in neuroblastoma and ganglioneuroblastoma is an independent predictor of poor outcome. Am J Pathol. 2012; 180(3):1223-1231.
36. Wang M, Zhou C, Sun Q, Cai R, Li Y, Wang D and Gong L. ALK amplification and protein expression predict inferior prognosis in neuroblastomas. Experimental and molecular pathology. 2013; 95(2):124-130.
37. Lamant L, Pulford K, Bischof D, Morris SW, Mason DY, Delsol G and Mariame B. Expression of the ALK tyrosine kinase gene in neuroblastoma. Am J Pathol. 2000; 156(5):1711-1721.
38. Schonherr C, Ruuth K, Yamazaki Y, Eriksson T, Christensen J, Palmer RH and Hallberg B. Activating ALK mutations found in neuroblastoma are inhibited by Crizotinib and NVP-TAE684. Biochem J. 2011; 440(3):405-413.
39. Chand D, Yamazaki Y, Ruuth K, Schonherr C, Martinsson T, Kogner P, Attiyeh EF, Maris J, Morozova O, Marra MA, Ohira M, Nakagawara A, Sandstrom PE, Palmer R and Hallberg B. Cell and Drosophila model systems define three classes of ALK mutations in neuroblastoma. Disease models & mechanisms. 2012.
40. Boutterin MC, Mazot P, Faure C, Doly S, Gervasi N, Tremblay ML and Vigny M. Control of ALK (wild type and mutated forms) phosphorylation: specific role of the phosphatase PTP1B. Cellular signalling. 2013; 25(6):1505-1513.
41. Raetz EA, Perkins SL, Carlson MA, Schooler KP, Carroll WL and Virshup DM. The nucleophosmin-anaplastic lymphoma kinase fusion protein induces c-Myc expression in pediatric anaplastic large cell lymphomas. Am J Pathol. 2002; 161(3):875-883.
42. Breit S and Schwab M. Suppression of MYC by high expression of NMYC in human neuroblastoma cells. J Neurosci Res. 1989; 24(1):21-28.
43. Stemple DL and Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell. 1992; 71(6):973-985.
44. Mazot P, Cazes A, Boutterin MC, Figueiredo A, Raynal V, Combaret V, Hallberg B, Palmer RH, Delattre O, Janoueix-Lerosey I and Vigny M. The constitutive activity of the ALK mutated at positions F1174 or R1275 impairs receptor trafficking. Oncogene. 2011; 30(17):2017-2025.
45. Pear WS, Miller JP, Xu L, Pui JC, Soffer B, Quackenbush RC, Pendergast AM, Bronson R, Aster JC, Scott ML and Baltimore D. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood. 1998; 92(10):3780-3792.
46. Muhlethaler-Mottet A, Bourloud KB, Auderset K, Joseph JM and Gross N. Drug-mediated sensitization to TRAIL-induced apoptosis in caspase-8-complemented neuroblastoma cells proceeds via activation of intrinsic and extrinsic pathways and caspase-dependent cleavage of XIAP, Bcl-x(L) and RIP. Oncogene. 2004; 23(32):5415-5425.
47. Muhlethaler-Mottet A, Flahaut M, Bourloud KB, Nardou K, Coulon A, Liberman J, Thome M and Gross N. Individual caspase-10 isoforms play distinct and opposing roles in the inapoptosisitiation of death receptor-mediated tumour cell. Cell Death and Disease. 2011; 2(1):e125.
48. Eliason JF, Aapro MS, Decrey D and Brink-Petersen M. Non-linearity of colony formation by human tumour cells from biopsy samples. Br J Cancer. 1985; 52(3):311-318.
49. Joseph JM, Gross N, Lassau N, Rouffiac V, Opolon P, Laudani L, Auderset K, Geay JF, Muhlethaler-Mottet A and Vassal G. In vivo echographic evidence of tumoral vascularization and microenvironment interactions in metastatic orthotopic human neuroblastoma xenografts. IntJCancer. 2005; 113(6):881-890.
50. Liberman J, Sartelet H, Flahaut M, Muhlethaler-Mottet A, Coulon A, Nyalendo C, Vassal G, Joseph JM and Gross N. Involvement of the CXCR7/CXCR4/CXCL12 Axis in the Malignant Progression of Human Neuroblastoma. PLoS ONE. 2012; 7(8):e43665.
51. Coulon A, Flahaut M, Muhlethaler-Mottet A, Meier R, Liberman J, Balmas-Bourloud K, Nardou K, Yan P, Tercier S, Joseph JM, Sommer L and Gross N. Functional sphere profiling reveals the complexity of neuroblastoma tumor-initiating cell model. Neoplasia. 2011; 13(10):991-1004.
52. Dai M, Wang P, Boyd AD, Kostov G, Athey B, Jones EG, Bunney WE, Myers RM, Speed TP, Akil H, Watson SJ and Meng F. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 2005; 33(20):e175.