MNT and Emerging Concepts of MNT-MYC Antagonism

Genes

Volumn 8, Issue 2, 2017, Pages

  Yang, Guang ^a   Hurlin, Peter J ^a,b  

^a SHRINERS HOSPITAL FOR CHILDREN   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

MAX; MLX; MLXIP; MNT; MXD; MYC; MYC antagonism

Indexed keywords

HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; MAX PROTEIN; MEMBRANE PROTEIN; MLX INTERACTING PROTEIN 1; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN E6; PROTEIN KINASE B; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR 1;

BINDING AFFINITY; BINDING SITE; CARCINOGENESIS; CELL PROLIFERATION; CHROMOSOME LOSS; GENE CONTROL; GENE LOCUS; GENE TARGETING; HUMAN; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; TRANSCRIPTION REGULATION;

EID: 85013384879     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes8020083     Document Type: Review

References (67)

1. Sheiness, D., Fanshier, L., Bishop, J.M. Identification of nucleotide sequences which may encode the oncogenic capacity of avian retrovirus MC29. J. Virol. 1978, 28, 600-610.
2. Roussel, M., Saule, S., Lagrou, C., Rommens, C., Beug, H., Graf, T., Stehelin, D. Three new types of viral oncogene of cellular origin specific for haematopoietic cell transformation. Nature 1979, 281, 452-455.
3. Gabay, M., Li, Y., Felsher, D.W. MYC activation is a hallmark of cancer initiation and maintenance. Cold Spring Harb. Perspect. Med. 2014, doi:10.1101/cshperspect.a014241.
4. Meyer, N., Penn, L.Z. Reflecting on 25 years with MYC. Nat. Rev. Cancer 2008, 8, 976-990.
5. Eilers, M., Eisenman, R.N. Myc’s broad reach. Genes Dev. 2008, 22, 2755-2766.
6. Dang, C.V. MYC on the path to cancer. Cell 2012, 149, 22-35.
7. Hurlin, P.J., Quéva, C., Eisenman, R.N. Mnt, a novel Max-interacting protein is coexpressed with MYC in proliferating cells and mediates repression at Myc binding sites. Genes Dev. 1997, 11, 44-58.
8. Hirotsune, S., Pack, S.D., Chong, S.S., Robbins, C.M., Pavan, W.J., Ledbetter, D.H., Wynshaw-Boris, A. Genomic organization of the murine Miller-Dieker/lissencephaly region: Conservation of linkage with the human region. Genome Res. 1997, 7, 625-634.
9. Meroni, G., Reymond, A., Alcalay, M., Borsani, G., Tanigami, A., Tonlorenzi, R., Lo Nigro, C., Messali, S., Zollo, M., Ledbetter, D.H., et al. Rox, a novel BHLHZip protein expressed in quiescent cells that heterodimerizes with Max, binds a non-canonical E box and acts as a transcriptional repressor. EMBO J. 1997, 16, 2892-2906.
10. Wynshaw-Boris, A. Lissencephaly and LIS1: Insights into the molecular mechanisms of neuronal migration and development. Clin. Genet. 2007, 72, 296-304.
11. Toyo-oka, K., Hirotsune, S., Gambello, M.J., Zhou, Z.-Q., Olson, L., Rosenfeld, M.G., Eisenman, R., Hurlin, P., Wynshaw-Boris, A. Loss of the Max-interacting protein Mnt in mice results in decreased viability, defective embryonic growth and craniofacial defects: Relevance to Miller-Dieker syndrome. Hum. Mol. Genet. 2004, 13, 1057-1067.
12. Ayer, D.E., Lawrence, Q.A., Eisenman, R.N. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell 1995, 80, 767-776.
13. Schreiber-Agus, N., Chin, L., Chen, K., Torres, R., Rao, G., Guida, P., Skoultchi, A.I., DePinho, R.A. An amino-terminal domain of Mxi1 mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN3. Cell 1995, 80, 777-786.
14. Hurlin, P.J., Quéva, C., Koskinen, P.J., Steingrímsson, E., Ayer, D.E., Copeland, N.G., Jenkins, N.A., Eisenman, R.N. Mad3 and Mad4: Novel Max-interacting transcriptional repressors that suppress c-myc dependent transformation and are expressed during neural and epidermal differentiation. EMBO J. 1995, 14, 5646-5659.
15. Grzenda, A., Lomberk, G., Zhang, J.-S., Urrutia, R. Sin3: Master scaffold and transcriptional corepressor. Biochim. Biophys. Acta 2009, 1789, 443-450.
16. Cowling, V.H., Cole, M.D. Mechanism of transcriptional activation by the Myc oncoproteins. Semin. Cancer Biol. 2006, 16, 242-252.
17. Hurlin, P.J., Zhou, Z.-Q., Toyo-oka, K., Ota, S., Walker, W.L., Hirotsune, S., Wynshaw-Boris, A. Deletion of Mnt leads to disrupted cell cycle control and tumorigenesis. EMBO J. 2003, 22, 4584-4596.
18. Nilsson, J.A., Maclean, K.H., Keller, U.B., Pendeville, H., Baudino, T.A., Cleveland, J.L. Mnt loss triggers Myc transcription targets, proliferation, apoptosis, and transformation. Mol. Cell. Biol. 2004, 24, 1560-1569.
19. Walker, W., Zhou, Z.-Q., Ota, S., Wynshaw-Boris, A., Hurlin, P.J. Mnt-Max to Myc-Max complex switching regulates cell cycle entry. J. Cell Biol. 2005, 169, 405-413.
20. Yang, H., Li, T.W.H., Ko, K.S., Xia, M., Lu, S.C. Switch from Mnt-Max to Myc-Max induces p53 and cyclin D1 expression and apoptosis during cholestasis in mouse and human hepatocytes. Hepatology 2009, 49, 860-870.
21. Wahlström, T., Belikov, S., Arsenian Henriksson, M. Chromatin dynamics at the hTERT promoter during transcriptional activation and repression by c-Myc and Mnt in Xenopus leavis oocytes. Exp. Cell Res. 2013, 319, 3160-3169.
22. Conacci-Sorrell, M., McFerrin, L., Eisenman, R.N. An overview of MYC and its interactome. Cold Spring Harb. Perspect. Med. 2014, doi:10.1101/cshperspect.a014357.
23. Toyo-oka, K., Bowen, T.J., Hirotsune, S., Li, Z., Jain, S., Ota, S., Escoubet-Lozach, L., Lozach, L.E., Garcia-Bassets, I., Bassett, I.G., et al. Mnt-deficient mammary glands exhibit impaired involution and tumors with characteristics of myc overexpression. Cancer Res. 2006, 66, 5565-5573.
24. Loo, L.W.M., Secombe, J., Little, J.T., Carlos, L.-S., Yost, C., Cheng, P.-F., Flynn, E.M., Edgar, B.A., Eisenman, R.N. The transcriptional repressor dMnt is a regulator of growth in Drosophila melanogaster. Mol. Cell. Biol. 2005, 25, 7078-7091.
25. Pierce, S.B., Yost, C., Anderson, S.A.R., Flynn, E.M., Delrow, J., Eisenman, R.N. Drosophila growth and development in the absence of dMyc and dMnt. Dev. Biol. 2008, 315, 303-316.
26. Orian, A., van Steensel, B., Delrow, J., Bussemaker, H.J., Li, L., Sawado, T., Williams, E., Loo, L.W.M., Cowley, S.M., Yost, C., et al. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev. 2003, 17, 1101-1114.
27. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489, 57-74.
28. Meroni, G., Cairo, S., Merla, G., Messali, S., Brent, R., Ballabio, A., Reymond, A. Mlx, a new Max-like BHLHZip family member: The center stage of a novel transcription factors regulatory pathway? Oncogene 2000, 19, 3266-3277.
29. Billin, A.N., Eilers, A.L., Queva, C., Ayer, D.E. Mlx, a novel Max-like BHLHZip protein that interacts with the Max network of transcription factors. J. Biol. Chem. 1999, 274, 36344-36350.
30. Billin, A.N., Eilers, A.L., Coulter, K.L., Logan, J.S., Ayer, D.E. MondoA, a novel basic helix-loop-helix-leucine zipper transcriptional activator that constitutes a positive branch of a max-like network. Mol. Cell. Biol. 2000, 20, 8845-8854.
31. Stoeckman, A.K., Ma, L., Towle, H.C. Mlx is the functional heteromeric partner of the carbohydrate response element-binding protein in glucose regulation of lipogenic enzyme genes. J. Biol. Chem. 2004, 279, 15662-15669.
32. O’Shea, J.M., Ayer, D.E. Coordination of nutrient availability and utilization by MAX- and MLX-centered transcription networks. Cold Spring Harb. Perspect. Med. 2013, doi:10.1101/cshperspect.a014258.
33. Carroll, P.A., Diolaiti, D., McFerrin, L., Gu, H., Djukovic, D., Du, J., Cheng, P.F., Anderson, S., Ulrich, M., Hurley, J.B., et al. Deregulated Myc Requires MondoA/Mlx for Metabolic Reprogramming and Tumorigenesis. Cancer Cell 2015, 27, 271-285.
34. Lin, C.Y., Lovén, J., Rahl, P.B., Paranal, R.M., Burge, C.B., Bradner, J.E., Lee, T.I., Young, R.A. Transcriptional Amplification in Tumor Cells with Elevated c-Myc. Cell 2012, 151, 56-67.
35. Nie, Z., Hu, G., Wei, G., Cui, K., Yamane, A., Resch, W., Wang, R., Green, D.R., Tessarollo, L., Casellas, R., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 2012, 151, 68-79.
36. Guccione, E., Martinato, F., Finocchiaro, G., Luzi, L., Tizzoni, L., Dall’ Olio, V., Zardo, G., Nervi, C., Bernard, L., Amati, B. Myc-binding-site recognition in the human genome is determined by chromatin context. Nat. Cell Biol. 2006, 8, 764-770.
37. Kim, J., Chu, J., Shen, X., Wang, J., Orkin, S.H. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008, 132, 1049-1061.
38. Sabò, A., Kress, T.R., Pelizzola, M., de Pretis, S., Gorski, M.M., Tesi, A., Morelli, M.J., Bora, P., Doni, M., Verrecchia, A., et al. Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis. Nature 2014, 511, 488-492.
39. Lorenzin, F., Benary, U., Baluapuri, A., Walz, S., Jung, L.A., von Eyss, B., Kisker, C., Wolf, J., Eilers, M., Wolf, E. Different promoter affinities account for specificity in MYC-dependent gene regulation. eLife 2016, doi:10.7554/eLife.15161.
40. Wolf, E., Lin, C.Y., Eilers, M., Levens, D.L. Taming of the beast: Shaping Myc-dependent amplification. Trends Cell Biol. 2015, 25, 241-248.
41. Kress, T.R., Sabò, A., Amati, B. MYC: Connecting selective transcriptional control to global RNA production. Nat. Rev. Cancer 2015, 15, 593-607.
42. Hurlin, P.J., Steingrìmsson, E., Copeland, N.G., Jenkins, N.A., Eisenman, R.N. Mga, a dual-specificity transcription factor that interacts with Max and contains a T-domain DNA-binding motif. EMBO J. 1999, 18, 7019-7028.
43. Dezfouli, S., Bakke, A., Huang, J., Wynshaw-Boris, A., Hurlin, P.J. Inflammatory disease and lymphomagenesis caused by deletion of the Myc antagonist Mnt in T cells. Mol. Cell. Biol. 2006, 26, 2080-2092.
44. Lo Nigro, C., Venesio, T., Reymond, A., Meroni, G., Alberici, P., Cainarca, S., Enrico, F., Stack, M., Ledbetter, D.H., Liscia, D.S., et al. The human ROX gene: Genomic structure and mutation analysis in human breast tumors. Genomics 1998, 49, 275-282.
45. Edelmann, J., Holzmann, K., Miller, F., Winkler, D., Bühler, A., Zenz, T., Bullinger, L., Kühn, M.W.M., Gerhardinger, A., Bloehdorn, J., et al. High-resolution genomic profiling of chronic lymphocytic leukemia reveals new recurrent genomic alterations. Blood 2012, 120, 4783-4794.
46. Vermeer, M.H., van Doorn, R., Dijkman, R., Mao, X., Whittaker, S., van Voorst Vader, P.C., Gerritsen, M.-J.P., Geerts, M.-L., Gellrich, S., Söderberg, O., et al. Novel and highly recurrent chromosomal alterations in Sézary syndrome. Cancer Res. 2008, 68, 2689-2698.
47. Boonk, S.E., Zoutman, W.H., Marie-Cardine, A., van der Fits, L., Out-Luiting, J.J., Mitchell, T.J., Tosi, I., Morris, S.L., Moriarty, B., Booken, N., et al. Evaluation of Immunophenotypic and Molecular Biomarkers for Sézary Syndrome Using Standard Operating Procedures: A Multicenter Study of 59 Patients. J. Investig. Dermatol. 2016, 136, 1364-1372.
48. Cvekl, A., Zavadil, J., Birshtein, B.K., Grotzer, M.A., Cvekl, A. Analysis of transcripts from 17p13.3 in medulloblastoma suggests ROX/MNT as a potential tumour suppressor gene. Eur. J. Cancer 2004, 40, 2525-2532.
49. Link, J.M., Ota, S., Zhou, Z.-Q., Daniel, C.J., Sears, R.C., Hurlin, P.J. A critical role for Mnt in Myc-driven T-cell proliferation and oncogenesis. Proc. Natl. Acad. Sci. USA 2012, 109, 19685-19690.
50. Murphy, D.J., Junttila, M.R., Pouyet, L., Karnezis, A., Shchors, K., Bui, D.A., Brown-Swigart, L., Johnson, L., Evan, G.I. Distinct thresholds govern Myc’s biological output in vivo. Cancer Cell 2008, 14, 447-457.
51. Vasilevsky, N.A., Ruby, C.E., Hurlin, P.J., Weinberg, A.D. OX40 engagement stabilizes Mxd4 and Mnt protein levels in antigen-stimulated T cells leading to an increase in cell survival. Eur. J. Immunol. 2011, 41, 1024-1034.
52. Terragni, J., Nayak, G., Banerjee, S., Medrano, J.-L., Graham, J.R., Brennan, J.F., Sepulveda, S., Cooper, G.M. The E-box binding factors Max/Mnt, MITF, and USF1 act coordinately with FoxO to regulate expression of proapoptotic and cell cycle control genes by phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3 signaling. J. Biol. Chem. 2011, 286, 36215-36227.
53. Popov, N., Wahlström, T., Hurlin, P.J., Henriksson, M. Mnt transcriptional repressor is functionally regulated during cell cycle progression. Oncogene 2005, 24, 8326-8337.
54. Zhang, Z., Sun, H., Dai, H., Walsh, R.M., Imakura, M., Schelter, J., Burchard, J., Dai, X., Chang, A.N., Diaz, R.L., et al. MicroRNA miR-210 modulates cellular response to hypoxia through the MYC antagonist MNT. Cell Cycle 2009, 8, 2756-2768.
55. Kulshreshtha, R., Ferracin, M., Wojcik, S.E., Garzon, R., Alder, H., Agosto-Perez, F.J., Davuluri, R., Liu, C.-G., Croce, C.M., Negrini, M., et al. A microRNA signature of hypoxia. Mol. Cell. Biol. 2007, 27, 1859-1867.
56. Ren, C.-X., Leng, R.-X., Fan, Y.-G., Pan, H.-F., Wu, C.-H., Ye, D.-Q. MicroRNA-210 and its theranostic potential. Expert Opin. Ther. Targets 2016, 20, 1325-1338.
57. Dang, C.V., Kim, J., Gao, P., Yustein, J. The interplay between MYC and HIF in cancer. Nat. Rev. Cancer 2008, 8, 51-56.
58. Yang, H., Li, T.W.H., Peng, J., Tang, X., Ko, K.S., Xia, M., Aller, M.-A. A mouse model of cholestasis-associated cholangiocarcinoma and transcription factors involved in progression. Gastroenterology 2011, 141, 378.e4-388.e4.
59. Yang, W., Wei, J., Guo, T., Shen, Y., Liu, F. Knockdown of miR-210 decreases hypoxic glioma stem cells stemness and radioresistance. Exp. Cell Res. 2014, 326, 22-35.
60. Bodempudi, V., Hergert, P., Smith, K., Xia, H., Herrera, J., Peterson, M., Khalil, W., Kahm, J., Bitterman, P.B., Henke, C.A. miR-210 promotes IPF fibroblast proliferation in response to hypoxia. Am. J. Physiol. Lung Cell. Mol. Physiol. 2014, 307, L283-L294.
61. Kapoor, I., Kanaujiya, J., Kumar, Y., Thota, J.R., Bhatt, M.L.B., Chattopadhyay, N., Sanyal, S., Trivedi, A.K. Proteomic discovery of MNT as a novel interacting partner of E3 ubiquitin ligase E6AP and a key mediator of myeloid differentiation. Oncotarget 2016, 7, 7640-7656.
62. Scheffner, M., Werness, B.A., Huibregtse, J.M., Levine, A.J., Howley, P.M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990, 63, 1129-1136.
63. Doorbar, J., Egawa, N., Griffin, H., Kranjec, C., Murakami, I. Human papillomavirus molecular biology and disease association. Rev. Med. Virol. 2015, 25, 2-23.
64. Wallace, N.A., Galloway, D.A. Novel Functions of the Human Papillomavirus E6 Oncoproteins. Annu. Rev. Virol. 2015, 2, 403-423.
65. Delgado, M.D., León, J. Myc Roles in Hematopoiesis and Leukemia. Genes Cancer 2010, 1, 605-616.
66. Hurlin, P.J., Foley, K.P., Ayer, D.E., Eisenman, R.N., Hanahan, D., Arbeit, J.M. Regulation of Myc and Mad during epidermal differentiation and HPV-associated tumorigenesis. Oncogene 1995, 11, 2487-2501.
67. Quéva, C., Hurlin, P.J., Foley, K.P., Eisenman, R.N. Sequential expression of the MAD family of transcriptional repressors during differentiation and development. Oncogene 1998, 16, 967-977.