Neuroblastoma (NB) is one of the most common malignant solid tumors in childhood, which derives from the sympathoadrenal lineage of the neural crest and exhibits extremely heterogeneous biological and clinical behaviors. The infant patients frequently undergo spontaneous regression even with metastatic disease, whereas the patients of more than one year of age who suffer from disseminated disease have a poor outcome despite intensive multimodal treatment. Spontaneous regression in favorable NBs has been proposed to be triggered by nerve growth factor (NGF) deficiency in the tumor with NGF dependency for survival, while aggressive NBs have defective apoptotic machinery which enables the tumor cells to evade apoptosis and confers the resistance to treatment. This paper reviews the molecules and pathways that have been recently identified to be involved in apoptotic cell death in NB and discusses their potential prospects for developing more effective therapeutic strategies against aggressive NB.
References
[1]
Maris, J.M. Recent advances in neuroblastoma. N. Engl. J. Med. 2010, 10, 2202–2211, doi:10.1056/NEJMra0804577.
[2]
Brodeur, G.M. Neuroblastoma: biological insights into a clinical enigma. Nat. Rev. Cancer 2003, 3, 203–216, doi:10.1038/nrc1014.
[3]
Breslow, N.; McCann, B. Statistical estimation of prognosis for children with neuroblastoma. Cancer Res. 1971, 31, 2098–2103.
[4]
Brodeur, G.M.; Pritchard, J.; Berthold, F.; Carlsen, N.L.; Castel, V.; Castelberry, R.P.; De Bernardi, B.; Evans, A.E.; Favrot, M.; Hedborg, F.; et al. Revisions of the international criteria for neuroblastoma diagnosis, Staging, And response to treatment. J. Clin. Oncol. 1993, 11, 1466–1477.
[5]
Shimada, H.; Ambros, I.M.; Dehner, L.P.; Hata, J.; Joshi, V.V.; Roald, B.; Stram, D.O.; Gerbing, R.B.; Lukens, J.N.; Matthay, K.K.; Castleberry, R.P. The International Neuroblastoma Pathology Classification (the Shimada system). Cancer 1999, 86, 364–372, doi:10.1002/(SICI)1097-0142(19990715)86:2<364::AID-CNCR21>3.0.CO;2-7.
[6]
Brodeur, G.; Seeger, R.C.; Schwab, M.; Varmus, H.E.; Bishop, J.M. Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science 1984, 224, 1121–1124.
[7]
Seeger, R.C.; Brodeur, G.M.; Sather, H.; Dalton, A.; Siegel, S.E.; Wong, K.Y.; Hammond, D. Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N. Engl. J. Med. 1985, 313, 1111–1116, doi:10.1056/NEJM198510313131802.
[8]
Look, A.T.; Hayes, F.A.; Nitschke, R.; McWilliams, N.B.; Green, A.A. Cellular DNA content as a predictor of response to chemotherapy in infants with unresectable neuroblastoma. N. Engl. J. Med. 1984, 311, 231–235, doi:10.1056/NEJM198407263110405.
[9]
The American Cancer Society. Available online: http://www.cancer.org (Accessed on 1 January 2013).
[10]
Hotchkiss, R.S.; Strasser, A.; McDunn, J.E.; Swanson, P.E. Cell death. N. Engl. J. Med. 2009, 361, 1570–1583, doi:10.1056/NEJMra0901217.
[11]
Henriquez, M.; Armisén, R.; Stutzin, A.; Quest, A.F. Cell death by necrosis, a regulated way to go. Curr. Mol. Med. 2008, 8, 187–206, doi:10.2174/156652408784221289.
[12]
Assun？？o Guimar？es, C.; Linden, R. Programmed cell deaths. Apoptosis and alternative deathstyles. Eur. J. Biochem. 2004, 271, 1638–1650, doi:10.1111/j.1432-1033.2004.04084.x.
[13]
Glick, D.; Barth, S.; Macleod, K.F. Autophagy: cellular and molecular mechanisms. J. Pathol. 2010, 221, 3–12, doi:10.1002/path.2697.
[14]
Fritsch, P.; Kerbl, R.; Lackner, H.; Urban, C. "Wait and see" strategy in localized neuroblastoma in infants: an option not only for cases detected by mass screening. Pediatr. Blood Cancer 2004, 43, 679–682, doi:10.1002/pbc.20126.
[15]
Hero, B.; Simon, T.; Spitz, R.; Ernestus, K.; Gnekow, A.K.; Scheel-Walter, H.G.; Schwabe, D.; Schilling, F.H.; Benz-Bohm, G.; Berthold, F. Localized infant neuroblastomas often show spontaneous regression: results of the prospective trials NB95-S and NB97. J. Clin. Oncol. 2008, 26, 1504–1510, doi:10.1200/JCO.2007.12.3349.
[16]
Oue, T.; Fukuzawa, M.; Kusafuka, T.; Kohmoto, Y.; Imura, K.; Nagahara, S.; Okada, A. In situ detection of DNA fragmentation and expression of bcl-2 in human neuroblastoma: relation to apoptosis and spontaneous regression. J. Pediatr. Surg. 1996, 31, 251–257, doi:10.1016/S0022-3468(96)90009-3.
[17]
Sartelet, H.; Ohta, S.; Barrette, S.; Rougemont, A.L.; Brevet, M.; Regairaz, M.; Harvey, I.; Bernard, C.; Fabre, M.; Gaboury, L.; et al. High level of apoptosis and low AKT activation in mass screening as opposed to standard neuroblastoma. Histopathology 2010, 56, 607–616, doi:10.1111/j.1365-2559.2010.03522.x.
[18]
Kitanaka, C.; Kato, K.; Ijiri, R.; Sakurada, K.; Tomiyama, A.; Noguchi, K.; Nagashima, Y.; Nakagawara, A.; Momoi, T.; Toyoda, Y.; et al. Increased Ras expression and caspase-independent neuroblastoma cell death: possible mechanism of spontaneous neuroblastoma regression. J. Natl. Cancer Inst. 2002, 94, 358–368, doi:10.1093/jnci/94.5.358.
[19]
Inoue, J.; Misawa, A.; Tanaka, Y.; Ichinose, S.; Sugino, Y.; Hosoi, H.; Sugimoto, T.; Imoto, I.; Inazawa, J. Lysosomal-associated protein multispanning transmembrane 5 gene (LAPTM5) is associated with spontaneous regression of neuroblastomas. PLoS One 2009, 4, e7099, doi:10.1371/journal.pone.0007099.
[20]
Eisenberg-Lerner, A.; Bialik, S.; Simon, H.U.; Kimchi, A. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ. 2009, 16, 966–975, doi:10.1038/cdd.2009.33.
[21]
Levi-Montalcini, R. The nerve growth factor 35 years later. Science 1987, 237, 1154–1162.
[22]
Deckwerth, T.L.; Johnson, E.M., Jr. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J. Cell Biol. 1993, 123, 1207–1222, doi:10.1083/jcb.123.5.1207.
[23]
Edwards, S.N.; Tolkovsky, A.M. Characterization of apoptosis in cultured rat sympathetic neurons after nerve growth factor withdrawal. J. Cell Biol. 1994, 124, 537–546, doi:10.1083/jcb.124.4.537.
[24]
Deshmukh, M.; Johnson, E.M., Jr. Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 1998, 21, 695–705, doi:10.1016/S0896-6273(00)80587-5.
[25]
Neame, S.J.; Rubin, L.L.; Philpott, K.L. Blocking cytochrome c activity within intact neurons inhibits apoptosis. J. Cell Biol. 1998, 142, 1583–1593, doi:10.1083/jcb.142.6.1583.
[26]
Wright, K.M.; Vaughn, A.E.; Deshmukh, M. Apoptosome dependent caspase-3 activation pathway is non-redundant and necessary for apoptosis in sympathetic neurons. Cell Death Differ. 2007, 14, 625–633, doi:10.1038/sj.cdd.4402024.
[27]
Johnson, D.; Lanahan, A.; Buck, C.R.; Sehgal, A.; Morgan, C.; Mercer, E.; Bothwell, M.; Chao, M. Expression and structure of the human NGF receptor. Cell 1986, 47, 545–554, doi:10.1016/0092-8674(86)90619-7.
[28]
Radeke, M.J.; Misko, T.P.; Hsu, C.; Herzenberg, L.A.; Shooter, E.M. Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 1987, 325, 593–597, doi:10.1038/325593a0.
[29]
Klein, R.; Jing, S.Q.; Nanduri, V.; O'Rourke, E.; Barbacid, M. The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 1991, 65, 189–197, doi:10.1016/0092-8674(91)90419-Y.
[30]
Hempstead, B.L.; Martin-Zanca, D.; Kaplan, D.R.; Parada, L.F.; Chao, M.V. High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 1991, 350, 678–683, doi:10.1038/350678a0.
[31]
He, X.L.; Garcia, K.C. Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 2004, 304, 870–875, doi:10.1126/science.1095190.
[32]
Nikoletopoulou, V.; Lickert, H.; Frade, J.M.; Rencurel, C.; Giallonardo, P.; Zhang, L.; Bibel, M.; Barde, Y.A. Neurotrophin receptors TrkA and TrkC cause neuronal death whereas TrkB does not. Nature 2010, 467, 59–63, doi:10.1038/nature09336.
[33]
Nakagawara, A.; Arima-Nakagawara, M.; Scavarda, N.J.; Azar, C.G.; Cantor, A.B.; Brodeur, G.M. Association between high levels of expression of the TRK gene and favorable outcome in human neuroblastoma. N. Engl. J. Med. 1993, 328, 847–854, doi:10.1056/NEJM199303253281205.
[34]
Christiansen, H.; Christiansen, N.M.; Wagner, F.; Altmannsberger, M.; Lampert, F. Neuroblastoma: Inverse relationship between expression of N-myc and NGF-r. Oncogene 1990, 5, 437–440.
[35]
Nakagawara, A.; Azar, C.G.; Scavarda, N.J.; Brodeur, G.M. Expression and function of TRK-B and BDNF in human neuroblastomas. Mol. Cell Biol. 1994, 14, 759–767.
[36]
Yamashiro, D.J.; Nakagawara, A.; Ikegaki, N.; Liu, X.G.; Brodeur, G.M. Expression of TrkC in favorable human neuroblastomas. Oncogene 1996, 12, 37–41.
[37]
Svensson, T.; Rydén, M.; Schilling, F.H.; Dominici, C.; Sehgal, R.; Ibá？ez, C.F.; Kogner, P. Coexpression of mRNA for the full-length neurotrophin receptor trk-C and trk-A in favourable neuroblastoma. Eur. J. Cancer 1997, 33, 2058–2063.
[38]
Tauszig-Delamasure, S.; Yu, L.Y.; Cabrera, J.R.; Bouzas-Rodriguez, J.; Mermet-Bouvier, C.; Guix, C.; Bordeaux, M.C.; Arum？e, U.; Mehlen, P. The TrkC receptor induces apoptosis when the dependence receptor notion meets the neurotrophin paradigm. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 13361–13366, doi:10.1073/pnas.0701243104.
[39]
Bouzas-Rodriguez, J.; Cabrera, J.R.; Delloye-Bourgeois, C.; Ichim, G.; Delcros, J.G.; Raquin, M.A.; Rousseau, R.; Combaret, V.; Bénard, J.; Tauszig-Delamasure, S.; et al. Neurotrophin-3 production promotes human neuroblastoma cell survival by inhibiting TrkC-induced apoptosis. J. Clin. Invest. 2010, 120, 850–858, doi:10.1172/JCI41013.
[40]
Rabizadeh, S.; Oh, J.; Zhong, L.T.; Yang, J.; Bitler, C.M.; Butcher, L.L.; Bredesen, D.E. Induction of apoptosis by the low-affinity NGF receptor. Science 1993, 261, 345–348.
[41]
Stiewe, T. The p53 family in differentiation and tumorigenesis. Nat. Rev. Cancer 2007, 7, 165–168, doi:10.1038/nrc2072.
[42]
Junttila, M.R.; Evan, G.I. p53—a Jack of all trades but master of none. Nat. Rev. Cancer 2009, 9, 821–829, doi:10.1038/nrc2728.
Aloyz, R.S.; Bamji, S.X.; Pozniak, C.D.; Toma, J.G.; Atwal, J.; Kaplan, D.R.; Miller, F.D. p53 is essential for developmental neuron death as regulated by the TrkA and p75 neurotrophin receptors. J. Cell Biol. 1998, 143, 1691–1703, doi:10.1083/jcb.143.6.1691.
[45]
Slack, R.S.; Belliveau, D.J.; Rosenberg, M.; Atwal, J.; Lochmüller, H.; Aloyz, R.; Haghighi, A.; Lach, B.; Seth, P.; Cooper, E.; et al. Adenovirus-mediated gene transfer of the tumor suppressor, p53, induces apoptosis in postmitotic neurons. J. Cell Biol. 1996, 135, 1085–1096, doi:10.1083/jcb.135.4.1085.
[46]
Vogel, K.S.; Parada, L.F. Sympathetic neuron survival and proliferation are prolonged by loss of p53 and neurofibromin. Mol. Cell Neurosci. 1998, 11, 19–28, doi:10.1006/mcne.1998.0670.
[47]
Jacobs, W.B.; Govoni, G.; Ho, D.; Atwal, J.K.; Barnabe-Heider, F.; Keyes, W.M.; Mills, A.A.; Miller, F.D.; Kaplan, D.R. p63 is an essential proapoptotic protein during neural development. Neuron 2005, 48, 743–756, doi:10.1016/j.neuron.2005.10.027.
[48]
Ozaki, T.; Nakagawara, A. p73, a sophisticated p53 family member in the cancer world. Cancer Sci. 2005, 96, 729–737, doi:10.1111/j.1349-7006.2005.00116.x.
[49]
Pietsch, E.C.; Sykes, S.M.; McMahon, S.B.; Murphy, M.E. The p53 family and programmed cell death. Oncogene 2008, 27, 6507–6521, doi:10.1038/onc.2008.315.
[50]
Pozniak, C.D.; Radinovic, S.; Yang, A.; McKeon, F.; Kaplan, D.R.; Miller, F.D. An anti-apoptotic role for the p53 family member, p73, during developmental neuron death. Science 2000, 289, 304–306, doi:10.1126/science.289.5477.304.
[51]
Lee, A.F.; Ho, D.K.; Zanassi, P.; Walsh, G.S.; Kaplan, D.R.; Miller, F.D. Evidence that DeltaNp73 promotes neuronal survival by p53-dependent and p53-independent mechanisms. J. Neurosci. 2004, 24, 9174–9184, doi:10.1523/JNEUROSCI.1588-04.2004.
[52]
Dugani, C.B.; Paquin, A.; Fujitani, M.; Kaplan, D.R.; Miller, F.D. p63 antagonizes p53 to promote the survival of embryonic neural precursor cells. J. Neurosci. 2009, 29, 6710–6721, doi:10.1523/JNEUROSCI.5878-08.2009.
[53]
Fujitani, M.; Cancino, G.I.; Dugani, C.B.; Weaver, I.C.; Gauthier-Fisher, A.; Paquin, A.; Mak, T.W.; Wojtowicz, M.J.; Miller, F.D.; Kaplan, D.R. TAp73 acts via the bHLH Hey2 to promote long-term maintenance of neural precursors. Curr. Biol. 2010, 20, 2058–2065, doi:10.1016/j.cub.2010.10.029.
Meletis, K.; Wirta, V.; Hede, S.M.; Nistér, M.; Lundeberg, J.; Frisén, J. p53 suppresses the self-renewal of adult neural stem cells. Development 2006, 133, 363–369.
[56]
Chesler, L.; Goldenberg, D.D.; Collins, R.; Grimmer, M.; Kim, G.E.; Tihan, T.; Nguyen, K.; Yakovenko, S.; Matthay, K.K.; Weiss, W.A. Chemotherapy-induced apoptosis in a transgenic model of neuroblastoma proceeds through p53 induction. Neoplasia 2008, 10, 1268–1274.
[57]
Lavoie, J.F.; Lesauteur, L.; Kohn, J.; Wong, J.; Furtoss, O.; Thiele, C.J.; Miller, F.D.; Kaplan, D.R. TrkA induces apoptosis of neuroblastoma cells and does so via a p53-dependent mechanism. J. Biol. Chem. 2005, 280, 29199–29207, doi:10.1074/jbc.M502364200.
[58]
Lo, W.D.; Akhmametyeva, E.M.; Zhu, L.; Friesen, P.D.; Chang, L.S. Induction of apoptosis by the p53-related p73 and partial inhibition by the baculovirus-encoded p35 in neuronal cells. Brain Res. Mol. Brain Res. 2003, 113, 1–12, doi:10.1016/S0169-328X(03)00052-4.
[59]
Horvilleur, E.; Bauer, M.; Goldschneider, D.; Mergui, X.; de la Motte, A.; Bénard, J.; Douc-Rasy, S.; Cappellen, D. p73alpha isoforms drive opposite transcriptional and post-transcriptional regulation of MYCN expression in neuroblastoma cells. Nucleic. Acids Res. 2008, 36, 4222–4232, doi:10.1093/nar/gkn394.
[60]
De Laurenzi, V.; Raschellá, G.; Barcaroli, D.; Annicchiarico-Petruzzelli, M.; Ranalli, M.; Catani, M.V.; Tanno, B.; Costanzo, A.; Levrero, M.; Melino, G. Induction of neuronal differentiation by p73 in a neuroblastoma cell line. J. Biol. Chem. 2000, 275, 15226–15231, doi:10.1074/jbc.275.20.15226.
[61]
Matthay, K.K.; Villablanca, J.G.; Seeger, R.C.; Stram, D.O.; Harris, R.E.; Ramsay, N.K.; Swift, P.; Shimada, H.; Black, C.T.; Brodeur, G.M.; et al. Treatment of high-risk neuroblastoma with intensive chemotherapy, Radiotherapy, Autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group. N. Engl. J. Med. 1999, 341, 1165–1173, doi:10.1056/NEJM199910143411601.
[62]
Casciano, I.; Mazzocco, K.; Boni, L.; Pagnan, G.; Banelli, B.; Allemanni, G.; Ponzoni, M.; Tonini, G.P.; Romani, M. Expression of DeltaNp73 is a molecular marker for adverse outcome in neuroblastoma patients. Cell Death Differ. 2002, 9, 246–251, doi:10.1038/sj.cdd.4400993.
[63]
Douc-Rasy, S.; Barrois, M.; Echeynne, M.; Kaghad, M.; Blanc, E.; Raguenez, G.; Goldschneider, D.; Terrier-Lacombe, M.J.; Hartmann, O.; Moll, U.; et al. DeltaN-p73alpha accumulates in human neuroblastic tumors. Am. J. Pathol. 2002, 160, 631–639, doi:10.1016/S0002-9440(10)64883-3.
[64]
Fillippovich, I.; Sorokina, N.; Gatei, M.; Haupt, Y.; Hobson, K.; Moallem, E.; Spring, K.; Mould, M.; McGuckin, M.A.; Lavin, M.F.; et al. Transactivation-deficient p73alpha (p73Deltaexon2) inhibits apoptosis and competes with p53. Oncogene 2001, 20, 514–522, doi:10.1038/sj.onc.1204118.
[65]
Nakagawa, T.; Takahashi, M.; Ozaki, T.; Watanabe, K.; Hayashi, S.; Hosoda, M.; Todo, S.; Nakagawara, A. Negative autoregulation of p73 and p53 by DeltaNp73 in regulating differentiation and survival of human neuroblastoma cells. Cancer Lett. 2003, 197, 105–109, doi:10.1016/S0304-3835(03)00090-9.
[66]
Irwin, M.; Marin, M.C.; Phillips, A.C.; Seelan, R.S.; Smith, D.I.; Liu, W.; Flores, E.R.; Tsai, K.Y.; Jacks, T.; Vousden, K.H.; et al. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000, 407, 645–648, doi:10.1038/35036614.
[67]
Persengiev, S.P.; Kondova, II.; Kilpatrick, D.L. E2F4 actively promotes the initiation and maintenance of nerve growth factor-induced cell differentiation. Mol. Cell Biol. 1999, 19, 6048–6056.
[68]
Nowak, K.; Killmer, K.; Gessner, C.; Lutz, W. E2F-1 regulates expression of FOXO1 and FOXO3a. Biochim. Biophys. Acta 2007, 1769, 244–252, doi:10.1016/j.bbaexp.2007.04.001.
[69]
Sim？es-Wüst, A.P.; Sigrist, B.; Belyanskaya, L.; Hopkins Donaldson, S.; Stahel, R.A.; Zangemeister-Wittke, U. DeltaNp73 antisense activates PUMA and induces apoptosis in neuroblastoma cells. J. Neurooncol. 2005, 72, 29–34, doi:10.1007/s11060-004-3118-8.
[70]
Ohira, M.; Oba, S.; Nakamura, Y.; Isogai, E.; Kaneko, S.; Nakagawa, A.; Hirata, T.; Kubo, H.; Goto, T.; Yamada, S.; et al. Expression profiling using a tumor-specific cDNA microarray predicts the prognosis of intermediate risk neuroblastomas. Cancer Cell 2005, 7, 337–350, doi:10.1016/j.ccr.2005.03.019.
[71]
Li, Y.; Ozaki, T.; Kikuchi, H.; Yamamoto, H.; Ohira, M.; Nakagawara, A. A novel HECT-type E3 ubiquitin protein ligase NEDL1 enhances the p53-mediated apoptotic cell death in its catalytic activity-independent manner. Oncogene 2008, 27, 3700–3709.
[72]
Miyazaki, K.; Fujita, T.; Ozaki, T.; Kato, C.; Kurose, Y.; Sakamoto, M.; Kato, S.; Goto, T.; Itoyama, Y.; Aoki, M.; et al. NEDL1, a novel ubiquitin-protein isopeptide ligase for dishevelled-1, targets mutant superoxide dismutase-1. J. Biol. Chem. 2004, 279, 11327–11335, doi:10.1074/jbc.M312389200.
[73]
Miller, F.D.; Pozniak, C.D.; Walsh, G.S. Neuronal life and death: an essential role for the p53 family. Cell Death Differ. 2000, 7, 880–888, doi:10.1038/sj.cdd.4400736.
[74]
Bredesen, D.E.; Mehlen, P.; Rabizadeh, S. Apoptosis and dependence receptors: a molecular basis for cellular addiction. Physiol. Rev. 2004, 84, 411–430.
[75]
Bredesen, D.E.; Mehlen, P.; Rabizadeh, S. Receptors that mediate cellular dependence. Cell Death Differ. 2005, 12, 1031–1043, doi:10.1038/sj.cdd.4401680.
[76]
Zhu, Y.; Li, Y.; Haraguchi, S.; Yu, M.; Ohira, M.; Ozaki, T.; Nakagawa, A.; Ushijima, T.; Isogai, E.; Koseki, H.; et al. Dependence receptor UNC5D mediates nerve growth factor depletion-induced neuroblastoma regression. J. Clin. Invest. 2013. in press.
Wang, H.; Ozaki, T.; Shamim Hossain, M.; Nakamura, Y.; Kamijo, T.; Xue, X.; Nakagawara, A. A newly identified dependence receptor UNC5H4 is induced during DNA damage-mediated apoptosis and transcriptional target of tumor suppressor p53. Biochem. Biophys. Res. Commun. 2008, 370, 594–598.
[79]
Reale, M.A.; Reyes-Mugica, M.; Pierceall, W.E.; Rubinstein, M.C.; Hedrick, L.; Cohn, S.L.; Nakagawara, A.; Brodeur, G.M.; Fearon, E.R. Loss of DCC expression in neuroblastoma is associated with disease dissemination. Clin. Cancer Res. 1996, 2, 1097–1102.
[80]
Kong, X.T.; Choi, S.H.; Inoue, A.; Takita, J.; Yokota, J.; Hanada, R.; Yamamoto, K.; Bessho, F.; Yanagisawa, M.; Hayashi, Y. Alterations of the tumour suppressor gene DCC in neuroblastoma. Eur. J. Cancer 1997, 33, 1962–1965, doi:10.1016/S0959-8049(97)00209-8.
[81]
Delloye-Bourgeois, C.; Fitamant, J.; Paradisi, A.; Cappellen, D.; Douc-Rasy, S.; Raquin, M.A.; Stupack, D.; Nakagawara, A.; Rousseau, R.; Combaret, V.; et al. Netrin-1 acts as a survival factor for aggressive neuroblastoma. J. Exp. Med. 2009, 206, 833–847, doi:10.1084/jem.20082299.
[82]
Nagai, M.; Ichimiya, S.; Ozaki, T.; Seki, N.; Mihara, M.; Furuta, S.; Ohira, M.; Tomioka, N.; Nomura, N.; Sakiyama, S.; et al. Identification of the full-length KIAA0591 gene encoding a novel kinesin-related protein which is mapped to the neuroblastoma suppressor gene locus at 1p36.2. Int. J. Oncol. 2000, 16, 907–916.
[83]
Ohira, M.; Kageyama, H.; Mihara, M.; Furuta, S.; Machida, T.; Shishikura, T.; Takayasu, H.; Islam, A.; Nakamura, Y.; Takahashi, M.; et al. Identification and characterization of a 500-kb homozygously deleted region at 1p36.2-p36.3 in a neuroblastoma cell line. Oncogene 2000, 19, 4302–4307, doi:10.1038/sj.onc.1203786.
[84]
Chen, Y.Z.; Soeda, E.; Yang, H.W.; Takita, J.; Chai, L.; Horii, A.; Inazawa, J.; Ohki, M.; Hayashi, Y. Homozygous deletion in a neuroblastoma cell line defined by a high-density STS map spanning human chromosome band 1p36. Genes Chromosomes Cancer 2001, 31, 326–332, doi:10.1002/gcc.1151.
[85]
Munirajan, A.K.; Ando, K.; Mukai, A.; Takahashi, M.; Suenaga, Y.; Ohira, M.; Koda, T.; Hirota, T.; Ozaki, T.; Nakagawara, A. KIF1Bbeta functions as a haploinsufficient tumor suppressor gene mapped to chromosome 1p36.2 by inducing apoptotic cell death. J. Biol. Chem. 2008, 283, 24426–24434, doi:10.1074/jbc.M802316200.
[86]
Hirokawa, N. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 1998, 279, 519–526, doi:10.1126/science.279.5350.519.
[87]
Goldstein, L.S.; Philp, A.V. The road less traveled: Emerging principles of kinesin motor utilization. Annu. Rev. Cell Dev. Biol. 1999, 15, 141–183, doi:10.1146/annurev.cellbio.15.1.141.
[88]
Schlisio, S.; Kenchappa, R.S.; Vredeveld, L.C.; George, R.E.; Stewart, R.; Greulich, H.; Shahriari, K.; Nguyen, N.V.; Pigny, P.; Dahia, P.L.; et al. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes Dev. 2008, 22, 884–893, doi:10.1101/gad.1648608.
[89]
Lee, S.; Nakamura, E.; Yang, H.; Wei, W.; Linggi, M.S.; Sajan, M.P.; Farese, R.V.; Freeman, R.S.; Carter, B.D.; Kaelin, W.G., Jr.; et al. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 2005, 8, 155–167, doi:10.1016/j.ccr.2005.06.015.
[90]
Strauchen, J.A. Germ-line mutations in nonsyndromic pheochromocytoma. N. Engl. J. Med. 2002, 347, 854–855, doi:10.1056/NEJM200209123471117.
[91]
Maher, E.R.; Eng, C. The pressure rises: update on the genetics of phaeochromocytoma. Hum. Mol. Genet. 2002, 11, 2347–2354.
[92]
Krona, C.; Ejesk？r, K.; Abel, F.; Kogner, P.; Bjelke, J.; Bj？rk, E.; Sj？berg, R.M.; Martinsson, T. Screening for gene mutations in a 500 kb neuroblastoma tumor suppressor candidate region in chromosome 1p; mutation and stage-specific expression in UBE4B/UFD2. Oncogene 2003, 22, 2343–2351, doi:10.1038/sj.onc.1206324.
[93]
Chuang, L.S.; Ito, Y. RUNX3 is multifunctional in carcinogenesis of multiple solid tumors. Oncogene 2010, 29, 2605–2615, doi:10.1038/onc.2010.88.
[94]
Chi, X.Z.; Yang, J.O.; Lee, K.Y.; Ito, K.; Sakakura, C.; Li, Q.L.; Kim, H.R.; Cha, E.J.; Lee, Y.H.; Kaneda, A.; et al. RUNX3 suppresses gastric epithelial cell growth by inducing p21(WAF1/Cip1) expression in cooperation with transforming growth factor {beta}-activated SMAD. Mol. Cell Biol. 2005, 25, 8097–9107, doi:10.1128/MCB.25.18.8097-8107.2005.
Ito, K.; Lim, A.C.; Salto-Tellez, M.; Motoda, L.; Osato, M.; Chuang, L.S.; Lee, C.W.; Voon, D.C.; Koo, J.K.; Wang, H.; et al. RUNX3 attenuates beta-catenin/T cell factors in intestinal tumorigenesis. Cancer Cell 2008, 14, 226–237, doi:10.1016/j.ccr.2008.08.004.
[97]
Yamada, C.; Ozaki, T.; Ando, K.; Suenaga, Y.; Inoue, K.; Ito, Y.; Okoshi, R.; Kageyama, H.; Kimura, H.; Miyazaki, M.; et al. RUNX3 modulates DNA damage-mediated phosphorylation of tumor suppressor p53 at Ser-15 and acts as a co-activator for p53. J. Biol. Chem. 2010, 285, 16693–16703, doi:10.1074/jbc.M109.055525.
[98]
Inoue, K.; Ito, K.; Osatom, M.; Lee, B.; Bae, S.C.; Ito, Y. The transcription factor Runx3 represses the neurotrophin receptor TrkB during lineage commitment of dorsal root ganglion neurons. J. Biol. Chem. 2007, 282, 24175–24184.
[99]
Inoue, K.; Ozaki, S.; Shiga, T.; Ito, K.; Masuda, T.; Okado, N.; Iseda, T.; Kawaguchi, S.; Ogawa, M.; Bae, S.C.; et al. Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nat. Neurosci. 2002, 5, 946–954, doi:10.1038/nn925.
[100]
Bagchi, A.; Papazoglu, C.; Wu, Y.; Capurso, D.; Brodt, M.; Francis, D.; Bredel, M.; Vogel, H.; Mills, A.A. CHD5 is a tumor suppressor at human 1p36. Cell 2007, 128, 459–475.
[101]
Bagchi, A.; Mills, A.A. The quest for the 1p36 tumor suppressor. Cancer Res. 2008, 68, 2551–2556, doi:10.1158/0008-5472.CAN-07-2095.
[102]
Mulero-Navarro, S.; Esteller, M. Chromatin remodeling factor CHD5 is silenced by promoter CpG island hypermethylation in human cancer. Epigenetics 2008, 3, 210–215, doi:10.4161/epi.3.4.6610.
[103]
Thompson, P.M.; Gotoh, T.; Kok, M.; White, P.S.; Brodeur, G.M. CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system. Oncogene 2003, 22, 1002–1011, doi:10.1038/sj.onc.1206211.
[104]
Garcia, I.; Mayol, G.; Rodríguez, E.; Su？ol, M.; Gershon, T.R.; Ríos, J.; Cheung, N.K.; Kieran, M.W.; George, R.E.; Perez-Atayde, A.R.; et al. Expression of the neuron-specific protein CHD5 is an independent marker of outcome in neuroblastoma. Mol. Cancer 2010, 9, 277, doi:10.1186/1476-4598-9-277.
[105]
Fujita, T.; Igarashi, J.; Okawa, E.R.; Gotoh, T.; Manne, J.; Kolla, V.; Kim, J.; Zhao, H.; Pawel, B.R.; London, W.B.; et al. CHD5, a tumor suppressor gene deleted from 1p36.31 in neuroblastomas. J. Natl. Cancer Inst. 2008, 100, 940–949, doi:10.1093/jnci/djn176.
[106]
Koyama, H.; Zhuang, T.; Light, J.E.; Kolla, V.; Higashi, M.; McGrady, P.W.; London, W.B.; Brodeur, G.M. Mechanisms of CHD5 Inactivation in neuroblastomas. Clin. Cancer Res. 2012, 18, 1588–1597, doi:10.1158/1078-0432.CCR-11-2644.
[107]
D'Angio, G.J.; Evans, A.E.; Koop, C.E. Special pattern of widespread neuroblastoma with a favourable prognosis. Lancet 1971, 1, 1046–1049, doi:10.1016/S0140-6736(71)91606-0.
[108]
Machida, T.; Fujita, T.; Ooo, M.L.; Ohira, M.; Isogai, E.; Mihara, M.; Hirato, J.; Tomotsune, D.; Hirata, T.; Fujimori, M.; et al. Increased expression of proapoptotic BMCC1, a novel gene with the BNIP2 and Cdc42GAP homology (BCH) domain, is associated with favorable prognosis in human neuroblastomas. Oncogene 2006, 25, 1931–1942, doi:10.1038/sj.onc.1209225.
[109]
Ando, K.; Ohira, M.; Ozaki, T.; Nakagawa, A.; Akazawa, K.; Suenaga, Y.; Nakamura, Y.; Koda, T.; Kamijo, T.; Murakami, Y.; et al. Expression of TSLC1, a candidate tumor suppressor gene mapped to chromosome 11q23, is downregulated in unfavorable neuroblastoma without promoter hypermethylation. Int. J. Cancer 2008, 123, 2087–2094, doi:10.1002/ijc.23776.
[110]
Nowacki, S.; Skowron, M.; Oberthuer, A.; Fagin, A.; Voth, H.; Brors, B.; Westermann, F.; Eggert, A.; Hero, B.; Berthold, F.; et al. Expression of the tumour suppressor gene CADM1 is associated with favourable outcome and inhibits cell survival in neuroblastoma. Oncogene 2008, 27, 3329–3338, doi:10.1038/sj.onc.1210996.
[111]
Mao, X.; Seidlitz, E.; Truant, R.; Hitt, M.; Ghosh, H.P. Re-expression of TSLC1 in a non-small-cell lung cancer cell line induces apoptosis and inhibits tumor growth. Oncogene 2004, 23, 5632–5642, doi:10.1038/sj.onc.1207756.
[112]
Lung, H.L.; Cheung, A.K.; Xie, D.; Cheng, Y.; Kwong, F.M.; Murakami, Y.; Guan, X.Y.; Sham, J.S.; Chua, D.; Protopopov, A.I.; et al. TSLC1 is a tumor suppressor gene associated with metastasis in nasopharyngeal carcinoma. Cancer Res. 2006, 66, 9385–9392, doi:10.1158/0008-5472.CAN-06-0590.
[113]
Hamano, S.; Ohira, M.; Isogai, E.; Nakada, K.; Nakagawara, A. Identification of novel human neuronal leucine-rich repeat (hNLRR) family genes and inverse association of expression of Nbla10449/hNLRR-1 and Nbla10677/hNLRR-3 with the prognosis of primary neuroblastomas. Int. J. Oncol. 2004, 24, 1457–1466.
[114]
Hossain, M.S.; Ozaki, T.; Wang, H.; Nakagawa, A.; Takenobu, H.; Ohira, M.; Kamijo, T.; Nakagawara, A. N-MYC promotes cell proliferation through a direct transactivation of neuronal leucine-rich repeat protein-1 (NLRR1) gene in neuroblastoma. Oncogene 2008, 27, 6075–6082, doi:10.1038/onc.2008.200.
[115]
Akter, J.; Takatori, A.; Hossain, M.S.; Ozaki, T.; Nakazawa, A.; Ohira, M.; Suenaga, Y.; Nakagawara, A. Expression of NLRR3 orphan receptor gene is negatively regulated by MYCN and Miz-1, and its downregulation is associated with unfavorable outcome in neuroblastoma. Clin. Cancer Res. 2011, 17, 6681–6692, doi:10.1158/1078-0432.CCR-11-0313.
[116]
Hossain, S.; Takatori, A.; Nakamura, Y.; Suenaga, Y.; Kamijo, T.; Nakagawara, A. NLRR1 enhances EGF-mediated MYCN induction in neuroblastoma and accelerates tumor growth in vivo. Cancer Res. 2012, 72, 4587–4596, doi:10.1158/0008-5472.CAN-12-0943.
[117]
Huang, S.; Laoukili, J.; Epping, M.T.; Koster, J.; H？lzel, M.; Westerman, B.A.; Nijkamp, W.; Hata, A.; Asgharzadeh, S.; Seeger, R.C.; et al. ZNF423 is critically required for retinoic acid-induced differentiation and is a marker of neuroblastoma outcome. Cancer Cell 2009, 15, 328–340, doi:10.1016/j.ccr.2009.02.023.
[118]
H？lzel, M.; Huang, S.; Koster, J.; Ora, I.; Lakeman, A.; Caron, H.; Nijkamp, W.; Xie, J.; Callens, T.; Asgharzadeh, S.; et al. NF1 is a tumor suppressor in neuroblastoma that determines retinoic acid response and disease outcome. Cell 2010, 142, 218–229, doi:10.1016/j.cell.2010.06.004.
[119]
Berwanger, B.; Hartmann, O.; Bergmann, E.; Bernard, S.; Nielsen, D.; Krause, M.; Kartal, A.; Flynn, D.; Wiedemeyer, R.; Schwab, M.; et al. Loss of a FYN-regulated differentiation and growth arrest pathway in advanced stage neuroblastoma. Cancer Cell 2002, 2, 377–386, doi:10.1016/S1535-6108(02)00179-4.
[120]
Teitz, T.; Wei, T.; Valentine, M.B.; Vanin, E.F.; Grenet, J.; Valentine, V.A.; Behm, F.G.; Look, A.T.; Lahti, J.M.; Kidd, V.J. Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat. Med. 2000, 6, 529–535, doi:10.1038/75007.
[121]
Fulda, S.; Küfer, M.U.; Meyer, E.; van Valen, F.; Dockhorn-Dworniczak, B.; Debatin, K.M. Sensitization for death receptor- or drug-induced apoptosis by re-expression of caspase-8 through demethylation or gene transfer. Oncogene 2001, 20, 5865–5877, doi:10.1038/sj.onc.1204750.
[122]
Yang, Q.; Kiernan, C.M.; Tian, Y.; Salwen, H.R.; Chlenski, A.; Brumback, B.A.; London, W.B.; Cohn, S.L. Methylation of CASP8, DCR2, and HIN-1 in neuroblastoma is associated with poor outcome. Clin. Cancer Res. 2007, 13, 3191–3197, doi:10.1158/1078-0432.CCR-06-2846.
[123]
Abe, M.; Ohira, M.; Kaneda, A.; Yagi, Y.; Yamamoto, S.; Kitano, Y.; Takato, T.; Nakagawara, A.; Ushijima, T. CpG island methylator phenotype is a strong determinant of poor prognosis in neuroblastomas. Cancer Res. 2005, 65, 828–834.
[124]
Gonzalez-Gomez, P.; Bello, M.J.; Lomas, J.; Arjona, D.; Alonso, M.E.; Ami？oso, C.; Lopez-Marin, I.; Anselmo, N.P.; Sarasa, J.L.; Gutierrez, M.; et al. Aberrant methylation of multiple genes in neuroblastic tumours. relationship with MYCN amplification and allelic status at 1p. Eur. J. Cancer 2003, 39, 1478–1485, doi:10.1016/S0959-8049(03)00312-5.
[125]
Fulda, S.; Poremba, C.; Berwanger, B.; H？cker, S.; Eilers, M.; Christiansen, H.; Hero, B.; Debatin, K.M. Loss of caspase-8 expression does not correlate with MYCN amplification, aggressive disease, or prognosis in neuroblastoma. Cancer Res. 2006, 66, 10016–10023, doi:10.1158/0008-5472.CAN-05-4079.
[126]
Miller, M.A.; Karacay, B.; Zhu, X.; O'Dorisio, M.S.; Sandler, A.D. Caspase 8L, a novel inhibitory isoform of caspase 8, is associated with undifferentiated neuroblastoma. Apoptosis 2006, 11, 15–24, doi:10.1007/s10495-005-3258-0.
[127]
van Noesel, M.M.; van Bezouw, S.; Salomons, G.S.; Vo？te, P.A.; Pieters, R.; Baylin, S.B.; Herman, J.G.; Versteeg, R. Tumor-specific down-regulation of the tumor necrosis factor-related apoptosis-inducing ligand decoy receptors DcR1 and DcR2 is associated with dense promoter hypermethylation. Cancer Res. 2002, 62, 2157–2161.
[128]
van Noesel, M.M.; van Bezouw, S.; Vo？te, P.A.; Herman, J.G.; Pieters, R.; Versteeg, R. Clustering of hypermethylated genes in neuroblastoma. Genes Chromosomes Cancer 2003, 38, 226–233, doi:10.1002/gcc.10278.
[129]
Yang, X.; Merchant, M.S.; Romero, M.E.; Tsokos, M.; Wexler, L.H.; Kontny, U.; Mackall, C.L.; Thiele, C.J. Induction of caspase 8 by interferon gamma renders some neuroblastoma (NB) cells sensitive to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) but reveals that a lack of membrane TR1/TR2 also contributes to TRAIL resistance in NB. Cancer Res. 2003, 63, 1122–1129.
[130]
Johnsen, J.I.; Pettersen, I.; Ponthan, F.; Sveinbj？rnsson, B.; Flaegstad, T.; Kogner, P. Synergistic induction of apoptosis in neuroblastoma cells using a combination of cytostatic drugs with interferon-gamma and TRAIL. Int. J. Oncol. 2004, 25, 1849–1857.
[131]
Weiss, W.A.; Aldape, K.; Mohapatra, G.; Feuerstein, B.G.; Bishop, J.M. Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J. 1997, 16, 2985–2995, doi:10.1093/emboj/16.11.2985.
[132]
Bell, E.; Chen, L.; Liu, T.; Marshall, G.M.; Lunec, J.; Tweddle, D.A. MYCN oncoprotein targets and their therapeutic potential. Cancer Lett. 2010, 293, 144–157, doi:10.1016/j.canlet.2010.01.015.
[133]
Ochiai, H.; Takenobu, H.; Nakagawa, A.; Yamaguchi, Y.; Kimura, M.; Ohira, M.; Okimoto, Y.; Fujimura, Y.; Koseki, H.; Kohno, Y.; et al. Bmi1 is a MYCN target gene that regulates tumorigenesis through repression of KIF1Bbeta and TSLC1 in neuroblastoma. Oncogene 2010, 29, 2681–2690, doi:10.1038/onc.2010.22.
[134]
Manohar, C.F.; Bray, J.A.; Salwen, H.R.; Madafiglio, J.; Cheng, A.; Flemming, C.; Marshall, G.M.; Norris, M.D.; Haber, M.; Cohn, S.L. MYCN-mediated regulation of the MRP1 promoter in human neuroblastoma. Oncogene 2004, 23, 753–762, doi:10.1038/sj.onc.1207151.
Paffhausen, T.; Schwab, M.; Westermann, F. Targeted MYCN expression affects cytotoxic potential of chemotherapeutic drugs in neuroblastoma cells. Cancer Lett. 2007, 250, 17–24, doi:10.1016/j.canlet.2006.09.010.
[137]
Chen, L.; Iraci, N.; Gherardi, S.; Gamble, L.D.; Wood, K.M.; Perini, G.; Lunec, J.; Tweddle, D.A. p53 is a direct transcriptional target of MYCN in neuroblastoma. Cancer Res. 2010, 70, 1377–1388, doi:10.1158/0008-5472.CAN-09-2598.
[138]
Seoane, J.; Le, H.V.; Massagué, J. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 2002, 419, 729–734, doi:10.1038/nature01119.
[139]
Slack, A.; Chen, Z.; Tonelli, R.; Pule, M.; Hunt, L.; Pession, A.; Shohet, J.M. The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 731–736.
[140]
Valsesia-Wittmann, S.; Magdeleine, M.; Dupasquier, S.; Garin, E.; Jallas, A.C.; Combaret, V.; Krause, A.; Leissner, P.; Puisieux, A. Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer Cell 2004, 6, 625–630, doi:10.1016/j.ccr.2004.09.033.
[141]
Fulda, S.; Lutz, W.; Schwab, M.; Debatin, K.M. MycN sensitizes neuroblastoma cells for drug-induced apoptosis. Oncogene 1999, 18, 1479–1486, doi:10.1038/sj.onc.1202435.
[142]
Cui, H.; Li, T.; Ding, H.F. Linking of N-Myc to death receptor machinery in neuroblastoma cells. J. Biol. Chem. 2005, 280, 9474–9481.
[143]
Clevers, H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127, 469–480, doi:10.1016/j.cell.2006.10.018.
[144]
Clevers, H.; Nusse, R. Wnt/β-catenin signaling and disease. Cell 2012, 149, 1192–1205, doi:10.1016/j.cell.2012.05.012.
Flahaut, M.; Meier, R.; Coulon, A.; Nardou, K.A.; Niggli, F.K.; Martinet, D.; Beckmann, J.S.; Joseph, J.M.; Mühlethaler-Mottet, A.; Gross, N. The Wnt receptor FZD1 mediates chemoresistance in neuroblastoma through activation of the Wnt/beta-catenin pathway. Oncogene 2009, 28, 2245–2256, doi:10.1038/onc.2009.80.
[147]
Vangipuram, S.D.; Buck, S.A.; Lyman, W.D. Wnt pathway activity confers chemoresistance to cancer stem-like cells in a neuroblastoma cell line. Tumour Biol. 2012, 33, 2173–2183, doi:10.1007/s13277-012-0478-0.
[148]
Blanc, E.; Roux, G.L.; Bénard, J.; Raguénez, G. Low expression of Wnt-5a gene is associated with high-risk neuroblastoma. Oncogene 2005, 24, 1277–1283, doi:10.1038/sj.onc.1208255.
[149]
Kühl, M. The WNT/calcium pathway: Biochemical mediators, Tools and future requirements. Front. Biosci. 2004, 9, 967–974, doi:10.2741/1307.
[150]
Blanc, E.; Goldschneider, D.; Douc-Rasy, S.; Bénard, J.; Raguénez, G. Wnt-5a gene expression in malignant human neuroblasts. Cancer Lett. 2005, 228, 117–123, doi:10.1016/j.canlet.2004.11.061.
[151]
Mossé, Y.P.; Wood, A.; Maris, J.M. Inhibition of ALK signaling for cancer therapy. Clin. Cancer Res. 2009, 15, 5609–5614, doi:10.1158/1078-0432.CCR-08-2762.
[152]
Mossé, Y.P.; Laudenslager, M.; Longo, L.; Cole, K.A.; Wood, A.; Attiyeh, E.F.; Laquaglia, M.J.; Sennett, R.; Lynch, J.E.; Perri, P.; et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008, 455, 930–935, doi:10.1038/nature07261.
[153]
Chen, Y.; Takita, J.; Choi, Y.L.; Kato, M.; Ohira, M.; Sanada, M.; Wang, L.; Soda, M.; Kikuchi, A.; Igarashi, T.; et al. Oncogenic mutations of ALK kinase in neuroblastoma. Nature 2008, 455, 971–974, doi:10.1038/nature07399.
[154]
Janoueix-Lerosey, I.; Lequin, D.; Brugières, L.; Ribeiro, A.; de Pontual, L.; Combaret, V.; Raynal, V.; Puisieux, A.; Schleiermacher, G.; Pierron, G.; et al. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 2008, 455, 967–970, doi:10.1038/nature07398.
[155]
George, R.E.; Sanda, T.; Hanna, M.; Fr？hling, S.; Luther, W., 2nd.; Zhang, J.; Ahn, Y.; Zhou, W.; London, W.B.; McGrady, P.; et al. Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature 2008, 455, 975–978, doi:10.1038/nature07397.
[156]
Osajima-Hakomori, Y.; Miyake, I.; Ohira, M.; Nakagawara, A.; Nakagawa, A.; Sakai, R. Biological role of anaplastic lymphoma kinase in neuroblastoma. Am. J. Pathol. 2005, 167, 213–222, doi:10.1016/S0002-9440(10)62966-5.
[157]
Ogawa, S.; Takita, J.; Sanada, M.; Hayashi, Y. Oncogenic mutations of ALK in neuroblastoma. Cancer Sci. 2011, 102, 302–308, doi:10.1111/j.1349-7006.2010.01825.x.
[158]
Bresler, S.C.; Wood, A.C.; Haglund, E.A.; Courtright, J.; Belcastro, L.T.; Plegaria, J.S.; Cole, K.; Toporovskaya, Y.; Zhao, H.; Carpenter, E.L.; et al. Differential inhibitor sensitivity of anaplastic lymphoma kinase variants found in neuroblastoma. Sci. Transl. Med. 2011, 3, 108ra114, doi:10.1126/scitranslmed.3002950.
[159]
Ola, M.S.; Nawaz, M.; Ahsan, H. Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol. Cell Biochem. 2011, 351, 41–58, doi:10.1007/s11010-010-0709-x.
[160]
Adams, J.M.; Cory, S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007, 26, 1324–1337, doi:10.1038/sj.onc.1210220.
[161]
Castle, V.P.; Heidelberger, K.P.; Bromberg, J.; Ou, X.; Dole, M.; Nu？ez, G. Expression of the apoptosis-suppressing protein bcl-2, in neuroblastoma is associated with unfavorable histology and N-myc amplification. Am. J. Pathol. 1993, 143, 1543–1550.
[162]
Ikegaki, N.; Katsumata, M.; Tsujimoto, Y.; Nakagawara, A.; Brodeur, G.M. Relationship between bcl-2 and myc gene expression in human neuroblastoma. Cancer Lett. 1995, 91, 161–168, doi:10.1016/0304-3835(95)03746-J.
[163]
Krajewski, S.; Krajewska, M.; Ehrmann, J.; Sikorska, M.; Lach, B.; Chatten, J.; Reed, J.C. Immunohistochemical analysis of Bcl-2, Bcl-X, Mcl-1, and Bax in tumors of central and peripheral nervous system origin. Am. J. Pathol. 1997, 150, 805–814.
[164]
Abel, F.; Sj？berg, R.M.; Nilsson, S.; Kogner, P.; Martinsson, T. Imbalance of the mitochondrial pro- and anti-apoptotic mediators in neuroblastoma tumours with unfavourable biology. Eur. J. Cancer 2005, 41, 635–646, doi:10.1016/j.ejca.2004.12.021.
[165]
Dole, M.G.; Jasty, R.; Cooper, M.J.; Thompson, C.B.; Nu？ez, G.; Castle, V.P. Bcl-xL is expressed in neuroblastoma cells and modulates chemotherapy-induced apoptosis. Cancer Res. 1995, 55, 2576–2582.
[166]
Dole, M.; Nu？ez, G.; Merchant, A.K.; Maybaum, J.; Rode, C.K.; Bloch, C.A.; Castle, V.P. Bcl-2 inhibits chemotherapy-induced apoptosis in neuroblastoma. Cancer Res. 1994, 54, 3253–3259.
[167]
Goldsmith, K.C.; Lestini, B.J.; Gross, M.; Ip, L.; Bhumbla, A.; Zhang, X.; Zhao, H.; Liu, X.; Hogarty, M.D. BH3 response profiles from neuroblastoma mitochondria predict activity of small molecule Bcl-2 family antagonists. Cell Death Differ. 2010, 17, 872–882, doi:10.1038/cdd.2009.171.
[168]
Goldsmith, K.C.; Gross, M.; Peirce, S.; Luyindula, D.; Liu, X.; Vu, A.; Sliozberg, M.; Guo, R.; Zhao, H.; Reynolds, C.P.; et al. Mitochondrial Bcl-2 family dynamics define therapy response and resistance in neuroblastoma. Cancer Res. 2012, 72, 2565–2577, doi:10.1158/0008-5472.CAN-11-3603.
[169]
Hadjidaniel, M.D.; Reynolds, C.P. Antagonism of cytotoxic chemotherapy in neuroblastoma cell lines by 13-cis-retinoic acid is mediated by the antiapoptotic Bcl-2 family proteins. Mol. Cancer Ther. 2010, 9, 3164–3174, doi:10.1158/1535-7163.MCT-10-0078.
[170]
Siddiquee, K.; Zhang, S.; Guida, W.C.; Blaskovich, M.A.; Greedy, B.; Lawrence, H.R.; Yip, M.L.; Jove, R.; McLaughlin, M.M.; Lawrence, N.J.; et al. Selective chemical probe inhibitor of Stat3, identified through structure-based virtual screening, Induces antitumor activity. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 7391–7396, doi:10.1073/pnas.0609757104.
[171]
Cosgrave, N.; Hill, A.D.; Young, L.S. Growth factor-dependent regulation of survivin by c-myc in human breast cancer. J. Mol. Endocrinol. 2006, 37, 377–390, doi:10.1677/jme.1.02118.
[172]
Lee, C.W.; Raskett, C.M.; Prudovsky, I.; Altieri, D.C. Molecular dependence of estrogen receptor-negative breast cancer on a notch-survivin signaling axis. Cancer Res. 2008, 68, 5273–5281, doi:10.1158/0008-5472.CAN-07-6673.
[173]
Kim, P.J.; Plescia, J.; Clevers, H.; Fearon, E.R.; Altieri, D.C. Survivin and molecular pathogenesis of colorectal cancer. Lancet 2003, 362, 205–209, doi:10.1016/S0140-6736(03)13910-4.
[174]
Kawakami, H.; Tomita, M.; Matsuda, T.; Ohta, T.; Tanaka, Y.; Fujii, M.; Hatano, M.; Tokuhisa, T.; Mori, N. Transcriptional activation of survivin through the NF-kappaB pathway by human T-cell leukemia virus type I tax. Int. J. Cancer 2005, 115, 967–974, doi:10.1002/ijc.20954.
[175]
Hoffman, W.H.; Biade, S.; Zilfou, J.T.; Chen, J.; Murphy, M. Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J. Biol. Chem. 2002, 277, 3247–3257.
[176]
Mirza, A.; McGuirk, M.; Hockenberry, T.N.; Wu, Q.; Ashar, H.; Black, S.; Wen, S.F.; Wang, L.; Kirschmeier, P.; Bishop, W.R.; et al. Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway. Oncogene 2002, 21, 2613–2622, doi:10.1038/sj.onc.1205353.
[177]
Jiang, Y.; Saavedra, H.I.; Holloway, M.P.; Leone, G.; Altura, R.A. Aberrant regulation of survivin by the RB/E2F family of proteins. J. Biol. Chem. 2004, 279, 40511–40520.
[178]
Wang, R.H.; Zheng, Y.; Kim, H.S.; Xu, X.; Cao, L.; Luhasen, T.; Lee, M.H.; Xiao, C.; Vassilopoulos, A.; Chen, W.; et al. Interplay among BRCA1, SIRT1, and Survivin during BRCA1-associated tumorigenesis. Mol. Cell 2008, 32, 11–20, doi:10.1016/j.molcel.2008.09.011.
[179]
Zhang, T.; Otevrel, T.; Gao, Z.; Gao, Z.; Ehrlich, S.M.; Fields, J.Z.; Boman, B.M. Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res. 2001, 61, 8664–8667.
[180]
Guha, M.; Altieri, D.C. Survivin as a global target of intrinsic tumor suppression networks. Cell Cycle 2009, 8, 2708–2710, doi:10.4161/cc.8.17.9457.
[181]
Islam, A.; Kageyama, H.; Takada, N.; Kawamoto, T.; Takayasu, H.; Isogai, E.; Ohira, M.; Hashizume, K.; Kobayashi, H.; Kaneko, Y.; et al. High expression of Survivin, mapped to 17q25, is significantly associated with poor prognostic factors and promotes cell survival in human neuroblastoma. Oncogene 2000, 19, 617–623, doi:10.1038/sj.onc.1203358.
[182]
Islam, A.; Kageyama, H.; Hashizume, K.; Kaneko, Y.; Nakagawara, A. Role of survivin, whose gene is mapped to 17q25, in human neuroblastoma and identification of a novel dominant-negative isoform, survivin-beta/2B. Med. Pediatr. Oncol. 2000, 35, 550–553, doi:10.1002/1096-911X(20001201)35:6<550::AID-MPO12>3.0.CO;2-Y.
[183]
Azuhata, T.; Scott, D.; Takamizawa, S.; Wen, J.; Davidoff, A.; Fukuzawa, M.; Sandler, A. The inhibitor of apoptosis protein survivin is associated with high-risk behavior of neuroblastoma. J. Pediatr. Surg. 2001, 36, 1785–1791, doi:10.1053/jpsu.2001.28839.
[184]
Miller, M.A.; Ohashi, K.; Zhu, X.; McGrady, P.; London, W.B.; Hogarty, M.; Sandler, A.D. Survivin mRNA levels are associated with biology of disease and patient survival in neuroblastoma: a report from the children's oncology group. J. Pediatr. Hematol. Oncol. 2006, 28, 412–417, doi:10.1097/01.mph.0000212937.00287.e5.
[185]
Fest, S.; Huebener, N.; Bleeke, M.; Durmus, T.; Stermann, A.; Woehler, A.; Baykan, B.; Zenclussen, A.C.; Michalsky, E.; Jaeger, I.S.; Preissner, R.; et al. Survivin minigene DNA vaccination is effective against neuroblastoma. Int. J. Cancer 2009, 125, 104–114, doi:10.1002/ijc.24291.
[186]
Rabbitts, T.H. LMO T-cell translocation oncogenes typify genes activated by chromosomal translocations that alter transcription and developmental processes. Genes Dev. 1998, 12, 2651–2657, doi:10.1101/gad.12.17.2651.
Visvader, J.E.; Venter, D.; Hahm, K.; Santamaria, M.; Sum, E.Y.; O'Reilly, L.; White, D.; Williams, R.; Armes, J.; Lindeman, G.J. The LIM domain gene LMO4 inhibits differentiation of mammary epithelial cells in vitro and is overexpressed in breast cancer. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 14452–14457, doi:10.1073/pnas.251547698.
[189]
Sum, E.Y.; Segara, D.; Duscio, B.; Bath, M.L.; Field, A.S.; Sutherland, R.L.; Lindeman, G.J.; Visvader, J.E. Overexpression of LMO4 induces mammary hyperplasia, promotes cell invasion, and is a predictor of poor outcome in breast cancer. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 7659–7664, doi:10.1073/pnas.0502990102.
[190]
Aoyama, M.; Ozaki, T.; Inuzuka, H.; Tomotsune, D.; Hirato, J.; Okamoto, Y.; Tokita, H.; Ohira, M.; Nakagawara, A. LMO3 interacts with neuronal transcription factor, HEN2, and acts as an oncogene in neuroblastoma. Cancer Res. 2005, 65, 4587–4597, doi:10.1158/0008-5472.CAN-04-4630.
[191]
Isogai, E.; Ohira, M.; Ozaki, T.; Oba, S.; Nakamura, Y.; Nakagawara, A. Oncogenic LMO3 collaborates with HEN2 to enhance neuroblastoma cell growth through transactivation of Mash1. PLoS One 2011, 6, e19297.
[192]
Gestblom, C.; Grynfeld, A.; Ora, I.; Ortoft, E.; Larsson, C.; Axelson, H.; Sandstedt, B.; Cserjesi, P.; Olson, E.N.; P？hlman, S. The basic helix-loop-helix transcription factor dHAND, a marker gene for the developing human sympathetic nervous system, is expressed in both high- and low-stage neuroblastomas. Lab. Invest. 1999, 79, 67–79.
[193]
Ichimiya, S.; Nimura, Y.; Seki, N.; Ozaki, T.; Nagase, T.; Nakagawara, A. Downregulation of hASH1 is associated with the retinoic acid-induced differentiation of human neuroblastoma cell lines. Med. Pediatr. Oncol. 2001, 36, 132–134.
[194]
Larsen, S.; Yokochi, T.; Isogai, E.; Nakamura, Y.; Ozaki, T.; Nakagawara, A. LMO3 interacts with p53 and inhibits its transcriptional activity. Biochem. Biophys. Res. Commun. 2010, 392, 252–257.
[195]
Wang, K.; Diskin, S.J.; Zhang, H.; Attiyeh, E.F.; Winter, C.; Hou, C.; Schnepp, R.W.; Diamond, M.; Bosse, K.; Mayes, P.A.; et al. Integrative genomics identifies LMO1 as a neuroblastoma oncogene. Nature 2011, 469, 216–220, doi:10.1038/nature09609.
