LMO1 Synergizes with MYCN to Promote Neuroblastoma Initiation and Metastasis

Cancer Cell

Volumn 32, Issue 3, 2017, Pages 310-323.e5

  Zhu, Shizhen ^a   Zhang, Xiaoling ^a   Weichert Leahey, Nina ^b   Dong, Zhiwei ^a   Zhang, Cheng ^c   Lopez, Gonzalo ^d   Tao, Ting ^b   He, Shuning ^b   Wood, Andrew C ^e   Oldridge, Derek ^d   Ung, Choong Yong ^c   van Ree, Janine H ^a   Khan, Amish ^a   Salazar, Brittany M ^a   Lummertz da Rocha, Edroaldo ^c   Zimmerman, Mark W ^b   Guo, Feng ^b   Cao, Hong ^a   Hou, Xiaonan ^f   Weroha, S John ^f   Perez Atayde, Antonio R ^b   Neuberg, Donna S ^g   Meves, Alexander ^f   McNiven, Mark A ^a   van Deursen, Jan M ^a   Li, Hu ^c   Maris, John M ^d,h,i   Look, A Thomas ^b   more..

^a MAYO CLINIC CANCER CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e UNIVERSITY OF AUCKLAND   (New Zealand)

^f MAYO CLINIC   (United States)

^g DANA FARBER CANCER INSTITUTE   (United States)

^h UNIVERSITY OF PENNSYLVANIA   (United States)

ⁱ UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

ECM; LMO1; metastasis; MYCN; neuroblastoma; tumorigenesis; zebrafish model

Indexed keywords

ARTICLE; CARCINOGENESIS; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE FUNCTION; HUMAN; HUMAN CELL; HYPERPLASIA; IN VIVO STUDY; LATENT PERIOD; LIM DOMAIN ONLY TRANSCRIPTIONAL COFACTOR GENE; METASTASIS; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; ONCOGENE; PATHOGENESIS; PENETRANCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; STEM CELL; TUMOR CELL; UPREGULATION; ZEBRA FISH; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC ANIMAL; TUMOR CELL LINE; TUMOR INVASION;

DNA BINDING PROTEIN; LIM PROTEIN; LMO1 PROTEIN, HUMAN; MYCN PROTEIN, HUMAN; N MYC PROTO ONCOGENE PROTEIN; TRANSCRIPTION FACTOR;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARCINOGENESIS; CELL LINE, TUMOR; CELL MOVEMENT; DNA-BINDING PROTEINS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPERPLASIA; LIM DOMAIN PROTEINS; MODELS, BIOLOGICAL; N-MYC PROTO-ONCOGENE PROTEIN; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEUROBLASTOMA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSGENES; ZEBRAFISH;

EID: 85028507715     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2017.08.002     Document Type: Article

References (59)

1. Ahmed, S., Goel, S., Khandwala, M., Agrawal, A., Chang, B., Simmons, I.G., Neuroblastoma with orbital metastasis: ophthalmic presentation and role of ophthalmologists. Eye (Lond.) 20 (2006), 466–470.
2. Anders, S., Huber, W., Differential expression analysis for sequence count data. Genome Biol., 11, 2010, R106.
3. Bach, I., The LIM domain: regulation by association. Mech. Dev. 91 (2000), 5–17.
4. Baker, A.M., Cox, T.R., Bird, D., Lang, G., Murray, G.I., Sun, X.F., Southall, S.M., Wilson, J.R., Erler, J.T., The role of lysyl oxidase in SRC-dependent proliferation and metastasis of colorectal cancer. J. Natl. Cancer Inst. 103 (2011), 407–424.
5. Barker, H.E., Cox, T.R., Erler, J.T., The rationale for targeting the LOX family in cancer. Nat. Rev. Cancer 12 (2012), 540–552.
6. Berry, T., Luther, W., Bhatnagar, N., Jamin, Y., Poon, E., Sanda, T., Pei, D., Sharma, B., Vetharoy, W.R., Hallsworth, A., et al. The ALK(F1174L) mutation potentiates the oncogenic activity of MYCN in neuroblastoma. Cancer Cell 22 (2012), 117–130.
7. Bray, N.L., Pimentel, H., Melsted, P., Pachter, L., Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34 (2016), 525–527.
8. Bresler, S.C., Weiser, D.A., Huwe, P.J., Park, J.H., Krytska, K., Ryles, H., Laudenslager, M., Rappaport, E.F., Wood, A.C., McGrady, P.W., et al. ALK mutations confer differential oncogenic activation and sensitivity to ALK inhibition therapy in neuroblastoma. Cancer Cell 26 (2014), 682–694.
9. Brodeur, G.M., Neuroblastoma: biological insights into a clinical enigma. Nat. Rev. Cancer 3 (2003), 203–216.
10. Clark, A.G., Vignjevic, D.M., Modes of cancer cell invasion and the role of the microenvironment. Curr. Opin. Cell Biol. 36 (2015), 13–22.
11. Dennis, M.S., Henzel, W.J., Pitti, R.M., Lipari, M.T., Napier, M.A., Deisher, T.A., Bunting, S., Lazarus, R.A., Platelet glycoprotein IIb-IIIa protein antagonists from snake venoms: evidence for a family of platelet-aggregation inhibitors. Proc. Natl. Acad. Sci. USA 87 (1990), 2471–2475.
12. Erler, J.T., Bennewith, K.L., Nicolau, M., Dornhofer, N., Kong, C., Le, Q.T., Chi, J.T., Jeffrey, S.S., Giaccia, A.J., Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440 (2006), 1222–1226.
13. Ganguly, K.K., Pal, S., Moulik, S., Chatterjee, A., Integrins and metastasis. Cell Adh. Migr. 7 (2013), 251–261.
14. Hartman, G.D., Egbertson, M.S., Halczenko, W., Laswell, W.L., Duggan, M.E., Smith, R.L., Naylor, A.M., Manno, P.D., Lynch, R.J., Zhang, G., et al. Non-peptide fibrinogen receptor antagonists. 1. Discovery and design of exosite inhibitors. J. Med. Chem. 35 (1992), 4640–4642.
15. Hay, E.D., Extracellular matrix. J. Cell Biol. 91 (1981), 205s–223s.
16. Hay, E.D., Extracellular matrix, cell skeletons, and embryonic development. Am. J. Med. Genet. 34 (1989), 14–29.
17. Heukamp, L.C., Thor, T., Schramm, A., De Preter, K., Kumps, C., De Wilde, B., Odersky, A., Peifer, M., Lindner, S., Spruessel, A., et al. Targeted expression of mutated ALK induces neuroblastoma in transgenic mice. Sci. Transl. Med., 4, 2012, 141ra191.
18. Hoye, A.M., Erler, J.T., Structural ECM components in the premetastatic and metastatic niche. Am. J. Physiol. Cell Physiol. 310 (2016), C955–C967.
19. Huth, J., Buchholz, M., Kraus, J.M., Schmucker, M., von Wichert, G., Krndija, D., Seufferlein, T., Gress, T.M., Kestler, H.A., Significantly improved precision of cell migration analysis in time-lapse video microscopy through use of a fully automated tracking system. BMC Cell Biol., 11, 2010, 24.
20. Hynes, R.O., Integrins: bidirectional, allosteric signaling machines. Cell 110 (2002), 673–687.
21. Hynes, R.O., Naba, A., Overview of the matrisome–an inventory of extracellular matrix constituents and functions. Cold Spring Harb. Perspect. Biol., 4, 2012, a004903.
22. Junqueira, L.C., Cossermelli, W., Brentani, R., Differential staining of collagens type I, II and III by Sirius Red and polarization microscopy. Arch. Histol. Jpn. 41 (1978), 267–274.
23. Kagan, H.M., Li, W., Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J. Cell Biochem. 88 (2003), 660–672.
24. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol., 14, 2013, R36.
25. Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., Schilling, T.F., Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995), 253–310.
26. Kirschmann, D.A., Seftor, E.A., Fong, S.F., Nieva, D.R., Sullivan, C.M., Edwards, E.M., Sommer, P., Csiszar, K., Hendrix, M.J., A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res. 62 (2002), 4478–4483.
27. Kurozumi, A., Goto, Y., Matsushita, R., Fukumoto, I., Kato, M., Nishikawa, R., Sakamoto, S., Enokida, H., Nakagawa, M., Ichikawa, T., Seki, N., Tumor-suppressive microRNA-223 inhibits cancer cell migration and invasion by targeting ITGA3/ITGB1 signaling in prostate cancer. Cancer Sci. 107 (2016), 84–94.
28. Langenau, D.M., Keefe, M.D., Storer, N.Y., Jette, C.A., Smith, A.C., Ceol, C.J., Bourque, C., Look, A.T., Zon, L.I., Co-injection strategies to modify radiation sensitivity and tumor initiation in transgenic zebrafish. Oncogene 27 (2008), 4242–4248.
29. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
30. Lapointe, J., Li, C., Higgins, J.P., van de Rijn, M., Bair, E., Montgomery, K., Ferrari, M., Egevad, L., Rayford, W., Bergerheim, U., et al. Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc. Natl. Acad. Sci. USA 101 (2004), 811–816.
31. Levental, K.R., Yu, H., Kass, L., Lakins, J.N., Egeblad, M., Erler, J.T., Fong, S.F., Csiszar, K., Giaccia, A., Weninger, W., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139 (2009), 891–906.
32. Li, X.Q., Lu, J.T., Tan, C.C., Wang, Q.S., Feng, Y.M., RUNX2 promotes breast cancer bone metastasis by increasing integrin alpha5-mediated colonization. Cancer Lett. 380 (2016), 78–86.
33. Lu, X., Wan, F., Zhang, H., Shi, G., Ye, D., ITGA2B and ITGA8 are predictive of prognosis in clear cell renal cell carcinoma patients. Tumour Biol. 37 (2016), 253–262.
34. Lutz, W., Stohr, M., Schurmann, J., Wenzel, A., Lohr, A., Schwab, M., Conditional expression of N-myc in human neuroblastoma cells increases expression of alpha-prothymosin and ornithine decarboxylase and accelerates progression into S-phase early after mitogenic stimulation of quiescent cells. Oncogene 13 (1996), 803–812.
35. Maris, J.M., Recent advances in neuroblastoma. N. Engl. J. Med. 362 (2010), 2202–2211.
36. Maris, J.M., Hogarty, M.D., Bagatell, R., Cohn, S.L., Neuroblastoma. Lancet 369 (2007), 2106–2120.
37. Matthews, J.M., Lester, K., Joseph, S., Curtis, D.J., LIM-domain-only proteins in cancer. Nat. Rev. Cancer 13 (2013), 111–122.
38. McCarroll, J.A., Phillips, P.A., Kumar, R.K., Park, S., Pirola, R.C., Wilson, J.S., Apte, M.V., Pancreatic stellate cell migration: role of the phosphatidylinositol 3-kinase(PI3-kinase) pathway. Biochem. Pharmacol. 67 (2004), 1215–1225.
39. Menke, A.L., Spitsbergen, J.M., Wolterbeek, A.P., Woutersen, R.A., Normal anatomy and histology of the adult zebrafish. Toxicol. Pathol. 39 (2011), 759–775.
40. Miranti, C.K., Brugge, J.S., Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4 (2002), E83–E90.
41. Naba, A., Clauser, K.R., Hoersch, S., Liu, H., Carr, S.A., Hynes, R.O., The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol. Cell. Proteomics, 11, 2012 M111 014647.
42. Nagata, M., Noman, A.A., Suzuki, K., Kurita, H., Ohnishi, M., Ohyama, T., Kitamura, N., Kobayashi, T., Uematsu, K., Takahashi, K., et al. ITGA3 and ITGB4 expression biomarkers estimate the risks of locoregional and hematogenous dissemination of oral squamous cell carcinoma. BMC Cancer, 13, 2013, 410.
43. Neely, G.G., Hess, A., Costigan, M., Keene, A.C., Goulas, S., Langeslag, M., Griffin, R.S., Belfer, I., Dai, F., Smith, S.B., et al. A genome-wide Drosophila screen for heat nociception identifies alpha2delta3 as an evolutionarily conserved pain gene. Cell 143 (2010), 628–638.
44. Oldridge, D.A., Wood, A.C., Weichert-Leahey, N., Crimmins, I., Sussman, R., Winter, C., McDaniel, L.D., Diamond, M., Hart, L.S., Zhu, S., et al. Genetic predisposition to neuroblastoma mediated by a LMO1 super-enhancer polymorphism. Nature 528 (2015), 418–421.
45. Park, J.R., Bagatell, R., London, W.B., Maris, J.M., Cohn, S.L., Mattay, K.K., Hogarty, M., Children's Oncology Group's 2013 blueprint for research: neuroblastoma. Pediatr. Blood Cancer 60 (2013), 985–993.
46. Paszek, M.J., Zahir, N., Johnson, K.R., Lakins, J.N., Rozenberg, G.I., Gefen, A., Reinhart-King, C.A., Margulies, S.S., Dembo, M., Boettiger, D., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8 (2005), 241–254.
47. Pugh, T.J., Morozova, O., Attiyeh, E.F., Asgharzadeh, S., Wei, J.S., Auclair, D., Carter, S.L., Cibulskis, K., Hanna, M., Kiezun, A., et al. The genetic landscape of high-risk neuroblastoma. Nat. Genet. 45 (2013), 279–284.
48. Pullar, C.E., Chen, J., Isseroff, R.R., PP2A activation by beta2-adrenergic receptor agonists: novel regulatory mechanism of keratinocyte migration. J. Biol. Chem. 278 (2003), 22555–22562.
49. Qin, L., Chen, X., Wu, Y., Feng, Z., He, T., Wang, L., Liao, L., Xu, J., Steroid receptor coactivator-1 upregulates integrin alpha(5) expression to promote breast cancer cell adhesion and migration. Cancer Res. 71 (2011), 1742–1751.
50. Renshaw, S.A., Trede, N.S., A model 450 million years in the making: zebrafish and vertebrate immunity. Dis. Models Mech. 5 (2012), 38–47.
51. Smith-Mungo, L.I., Kagan, H.M., Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol. 16 (1998), 387–398.
52. Smith, S.J., Diehl, N.N., Smith, B.D., Mohney, B.G., Incidence, ocular manifestations, and survival in children with neuroblastoma: a population-based study. Am. J. Ophthalmol. 149 (2010), 677–682.e2.
53. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
54. Sweat, F., Puchtler, H., Rosenthal, S.I., Sirius Red F3ba as a stain for connective tissue. Arch. Pathol. 78 (1964), 69–72.
55. Tcheng, J.E., Talley, J.D., O'Shea, J.C., Gilchrist, I.C., Kleiman, N.S., Grines, C.L., Davidson, C.J., Lincoff, A.M., Califf, R.M., Jennings, L.K., et al. Clinical pharmacology of higher dose eptifibatide in percutaneous coronary intervention (the PRIDE study). Am. J. Cardiol. 88 (2001), 1097–1102.
56. 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 469 (2011), 216–220.
57. Wang, C., Gong, B., Bushel, P.R., Thierry-Mieg, J., Thierry-Mieg, D., Xu, J., Fang, H., Hong, H., Shen, J., Su, Z., et al. The concordance between RNA-seq and microarray data depends on chemical treatment and transcript abundance. Nat. Biotechnol. 32 (2014), 926–932.
58. Wong, C.C., Tse, A.P., Huang, Y.P., Zhu, Y.T., Chiu, D.K., Lai, R.K., Au, S.L., Kai, A.K., Lee, J.M., Wei, L.L., et al. Lysyl oxidase-like 2 is critical to tumor microenvironment and metastatic niche formation in hepatocellular carcinoma. Hepatology 60 (2014), 1645–1658.
59. Zhu, S., Lee, J.S., Guo, F., Shin, J., Perez-Atayde, A.R., Kutok, J.L., Rodig, S.J., Neuberg, D.S., Helman, D., Feng, H., et al. Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell 21 (2012), 362–373.