HOPX: The Unusual Homeodomain-Containing Protein

Journal of Investigative Dermatology

Volumn 136, Issue 5, 2016, Pages 905-911

  Mariotto, Anita ^a   Pavlova, Olesya ^a   Park, Hyun Sook ^a   Huber, Marcel ^a   Hohl, Daniel ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN ONLY PROTEIN HOMEOBOX; HOMEODOMAIN PROTEIN; UNCLASSIFIED DRUG;

CELL DIFFERENTIATION; EPIDERMIS; HEART DEVELOPMENT; HUMAN; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; STEM CELL; TISSUES; ANIMAL; CELL PROLIFERATION; COMPARATIVE STUDY; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETICS; HOMEOBOX; MOUSE; PATHOPHYSIOLOGY; SENSITIVITY AND SPECIFICITY; SKIN TUMOR; TUMOR CELL CULTURE;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; HUMANS; MICE; SENSITIVITY AND SPECIFICITY; SKIN NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 84978159555     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1016/j.jid.2016.01.032     Document Type: Review

References (75)

1. Abrous, D.N., Koehl, M., Le Moal, M., Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85 (2005), 523–569.
2. Akam, M., The molecular basis for metameric pattern in the Drosophila embryo. Development 101 (1987), 1–22.
3. Albrecht, I., Niesner, U., Janke, M., Menning, A., Loddenkemper, C., Kuhl, A.A., et al. Persistence of effector memory Th1 cells is regulated by Hopx. Eur J Immunol 40 (2010), 2993–3006.
4. Asanoma, K., Kato, H., Yamaguchi, S., Shin, C.H., Liu, Z.P., Kato, K., et al. HOP/NECC1, a novel regulator of mouse trophoblast differentiation. J Biol Chem 282 (2007), 24065–24074.
5. Asanoma, K., Matsuda, T., Kondo, H., Kato, K., Kishino, T., Niikawa, N., et al. NECC1, a candidate choriocarcinoma suppressor gene that encodes a homeodomain consensus motif. Genomics 81 (2003), 15–25.
6. Attwooll, C., Oddi, S., Cartwright, P., Prosperini, E., Agger, K., Steensgaard, P., et al. A novel repressive E2F6 complex containing the polycomb group protein, EPC1, that interacts with EZH2 in a proliferation-specific manner. J Biol Chem 280 (2005), 1199–1208.
7. Berger, M.F., Badis, G., Gehrke, A.R., Talukder, S., Philippakis, A.A., Pena-Castillo, L., et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133 (2008), 1266–1276.
8. Burglin, T.R., Homeodomain subtypes and functional diversity. Subcell Biochem 52 (2011), 95–122.
9. Chen, C.Y., Schwartz, R.J., Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac alpha-actin gene transcription. Mol Cell Biol 16 (1996), 6372–6384.
10. Chen, F., Kook, H., Milewski, R., Gitler, A.D., Lu, M.M., Li, J., et al. Hop is an unusual homeobox gene that modulates cardiac development. Cell 110 (2002), 713–723.
11. Chen, Y., Pacyna-Gengelbach, M., Deutschmann, N., Niesporek, S., Petersen, I., Homeobox gene HOP has a potential tumor suppressive activity in human lung cancer. Int J Cancer 121 (2007), 1021–1027.
12. Chen, Y., Petersen, S., Pacyna-Gengelbach, M., Pietas, A., Petersen, I., Identification of a novel homeobox-containing gene, LAGY, which is downregulated in lung cancer. Oncology 64 (2003), 450–458.
13. Chen, Y., Yang, L., Cui, T., Pacyna-Gengelbach, M., Petersen, I., HOPX is methylated and exerts tumour suppressive function through Ras-induced senescence in human lung cancer. J Pathol 235 (2015), 397–407.
14. Cheung, W.K., Zhao, M., Liu, Z., Stevens, L.E., Cao, P.D., Fang, J.E., et al. Control of alveolar differentiation by the lineage transcription factors GATA6 and HOPX inhibits lung adenocarcinoma metastasis. Cancer Cell 23 (2013), 725–738.
15. De Toni, A., Zbinden, M., Epstein, J.A., Ruiz i Altaba, A., Prochiantz, A., Caille, I., Regulation of survival in adult hippocampal and glioblastoma stem cell lineages by the homeodomain-only protein HOP. Neural Dev, 3, 2008, 13.
16. Descatoire, M., Weller, S., Irtan, S., Feuillard, J., Storck, S., Guiochon-Mantel, A., et al. Identification of a human splenic marginal zone B cell precursor with NOTCH2-dependent differentiation properties. J Exp Med 211 (2014), 987–1000.
17. Doyon, Y., Selleck, W., Lane, W.S., Tan, S., Cote, J., Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol Cell Biol 24 (2004), 1884–1896.
18. Duboule, D., Guidebook to the homeobox genes. 1994, Oxford University Press, Oxford.
19. Durocher, D., Charron, F., Warren, R., Schwartz, R.J., Nemer, M., The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. EMBO J 16 (1997), 5687–5696.
20. Fishman, G.I., Understanding conduction system development: a hop, skip and jump away?. Circ Res 96 (2005), 809–811.
21. Fuchs, E., The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137 (2009), 811–819.
22. Greif, P.A., Konstandin, N.P., Metzeler, K.H., Herold, T., Pasalic, Z., Ksienzyk, B., et al. RUNX1 mutations in cytogenetically normal acute myeloid leukemia are associated with a poor prognosis and up-regulation of lymphoid genes. Haematologica 97 (2012), 1909–1915.
23. Harada, Y., Kijima, K., Shinmura, K., Sakata, M., Sakuraba, K., Yokomizo, K., et al. Methylation of the homeobox gene, HOPX, is frequently detected in poorly differentiated colorectal cancer. Anticancer Res 31 (2011), 2889–2892.
24. Hawiger, D., Wan, Y.Y., Eynon, E.E., Flavell, R.A., The transcription cofactor Hopx is required for regulatory T cell function in dendritic cell-mediated peripheral T cell unresponsiveness. Nat Immunol 11 (2010), 962–968.
25. Hayashi, S., Scott, M.P., What determines the specificity of action of Drosophila homeodomain proteins?. Cell 63 (1990), 883–894.
26. Holland, P.W., Booth, H.A., Bruford, E.A., Classification and nomenclature of all human homeobox genes. BMC Biol, 5, 2007, 47.
27. Holland, P.W., Takahashi, T., The evolution of homeobox genes: implications for the study of brain development. Brain Res Bull 66 (2005), 484–490.
28. Ismat, F.A., Zhang, M., Kook, H., Huang, B., Zhou, R., Ferrari, V.A., et al. Homeobox protein Hop functions in the adult cardiac conduction system. Circ Res 96 (2005), 898–903.
29. Jain, R., Li, D., Gupta, M., Manderfield, L.J., Ifkovits, J.L., Wang, Q., et al. HEART DEVELOPMENT. Integration of Bmp and Wnt signaling by Hopx specifies commitment of cardiomyoblasts. Science, 348, 2015, aaa6071.
30. Jones, A., Opejin, A., Henderson, J.G., Gross, C., Jain, R., Epstein, J.A., et al. Peripherally induced tolerance depends on peripheral regulatory T cells that require Hopx to inhibit intrinsic IL-2 expression. J Immunol 195 (2015), 1489–1497.
31. Katoh, H., Yamashita, K., Waraya, M., Margalit, O., Ooki, A., Tamaki, H., et al. Epigenetic silencing of HOPX promotes cancer progression in colorectal cancer. Neoplasia 14 (2012), 559–571.
32. Kaufman, T.C., Lewis, R., Wakimoto, B., Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: the homoeotic gene complex in polytene chromosome interval 84a-B. Genetics 94 (1980), 115–133.
33. Kee, H.J., Kim, J.R., Nam, K.I., Park, H.Y., Shin, S., Kim, J.C., et al. Enhancer of polycomb1, a novel homeodomain only protein-binding partner, induces skeletal muscle differentiation. J Biol Chem 282 (2007), 7700–7709.
34. Kissinger, C.R., Liu, B., Martin-Blanco, E., Kornberg, T.B., Pabo, C.O., Crystal structure of an engrailed homeodomain-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain-DNA interactions. Cell 63 (1990), 579–590.
35. Kook, H., Epstein, J.A., Hopping to the beat. Hop regulation of cardiac gene expression. Trends Cardiovasc Med 13 (2003), 261–264.
36. Kook, H., Lepore, J.J., Gitler, A.D., Lu, M.M., Wing-Man Yung, W., Mackay, J., et al. Cardiac hypertrophy and histone deacetylase-dependent transcriptional repression mediated by the atypical homeodomain protein Hop. J Clin Invest 112 (2003), 863–871.
37. Kook, H., Yung, W.W., Simpson, R.J., Kee, H.J., Shin, S., Lowry, J.A., et al. Analysis of the structure and function of the transcriptional coregulator HOP. Biochemistry 45 (2006), 10584–10590.
38. Kovarova, D., Plachy, J., Kosla, J., Trejbalova, K., Cermak, V., Hejnar, J., Downregulation of HOPX controls metastatic behavior in sarcoma cells and identifies genes associated with metastasis. Mol Cancer Res 11 (2013), 1235–1247.
39. Laughon, A., Scott, M.P., Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature 310 (1984), 25–31.
40. Lemaire, F., Millon, R., Muller, D., Rabouel, Y., Bracco, L., Abecassis, J., et al. Loss of HOP tumour suppressor expression in head and neck squamous cell carcinoma. Br J Cancer 91 (2004), 258–261.
41. Lewis, E.B., A gene complex controlling segmentation in Drosophila. Nature 276 (1978), 565–570.
42. Li, N., Yousefi, M., Nakauka-Ddamba, A., Jain, R., Tobias, J., Epstein, J.A., et al. Single-cell analysis of proxy reporter allele-marked epithelial cells establishes intestinal stem cell hierarchy. Stem Cell Reports 3 (2014), 876–891.
43. Liu, C., Glasser, S.W., Wan, H., Whitsett, J.A., GATA-6 and thyroid transcription factor-1 directly interact and regulate surfactant protein-C gene expression. J Biol Chem 277 (2002), 4519–4525.
44. Liu, F., Levin, M.D., Petrenko, N.B., Lu, M.M., Wang, T., Yuan, L.J., et al. Histone-deacetylase inhibition reverses atrial arrhythmia inducibility and fibrosis in cardiac hypertrophy independent of angiotensin. J Mol Cell Cardiol 45 (2008), 715–723.
45. Lledo, P.M., Alonso, M., Grubb, M.S., Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7 (2006), 179–193.
46. McGinnis, W., Garber, R.L., Wirz, J., Kuroiwa, A., Gehring, W.J., A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37 (1984), 403–408.
47. McGinnis, W., Levine, M.S., Hafen, E., Kuroiwa, A., Gehring, W.J., A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308 (1984), 428–433.
48. Muhlfriedel, S., Kirsch, F., Gruss, P., Stoykova, A., Chowdhury, K., A roof plate-dependent enhancer controls the expression of Homeodomain only protein in the developing cerebral cortex. Dev Biol 283 (2005), 522–534.
49. Noyes, M.B., Christensen, R.G., Wakabayashi, A., Stormo, G.D., Brodsky, M.H., Wolfe, S.A., Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133 (2008), 1277–1289.
50. Obarzanek-Fojt, M., Favre, B., Kypriotou, M., Ryser, S., Huber, M., Hohl, D., Homeodomain-only protein HOP is a novel modulator of late differentiation in keratinocytes. Eur J Cell Biol 90 (2011), 279–290.
51. Ooki, A., Yamashita, K., Kikuchi, S., Sakuramoto, S., Katada, N., Kokubo, K., et al. Potential utility of HOP homeobox gene promoter methylation as a marker of tumor aggressiveness in gastric cancer. Oncogene 29 (2010), 3263–3275.
52. Otting, G., Qian, Y.Q., Billeter, M., Muller, M., Affolter, M., Gehring, W.J., et al. Protein–DNA contacts in the structure of a homeodomain–DNA complex determined by nuclear magnetic resonance spectroscopy in solution. EMBO J 9 (1990), 3085–3092.
53. Peters, T.J., Chapman, B.M., Wolfe, M.W., Soares, M.J., Placental lactogen-I gene activation in differentiating trophoblast cells: extrinsic and intrinsic regulation involving mitogen-activated protein kinase signaling pathways. J Endocrinol 165 (2000), 443–456.
54. Qian, Y., Billeter, M., Otting, G., Müller, M., Gehring, W., Wüthrich, K., The structure of the Antennapedia homeodomain determined by NMR spectroscopy in solution: comparison with prokaryotic repressors. Cell 59 (1989), 573–580.
55. Ryan, J.F., Burton, P.M., Mazza, M.E., Kwong, G.K., Mullikin, J.C., Finnerty, J.R., The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol, 7, 2006, R64.
56. Scott, M.P., Weiner, A.J., Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci USA 81 (1984), 4115–4119.
57. Sepulveda, J.L., Vlahopoulos, S., Iyer, D., Belaguli, N., Schwartz, R.J., Combinatorial expression of GATA4, Nkx2-5, and serum response factor directs early cardiac gene activity. J Biol Chem 277 (2002), 25775–25782.
58. Shepherd, J.C., McGinnis, W., Carrasco, A.E., De Robertis, E.M., Gehring, W.J., Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins. Nature 310 (1984), 70–71.
59. Shimono, Y., Murakami, H., Hasegawa, Y., Takahashi, M., RET finger protein is a transcriptional repressor and interacts with enhancer of polycomb that has dual transcriptional functions. J Biol Chem 275 (2000), 39411–39419.
60. Shin, C.H., Liu, Z.P., Passier, R., Zhang, C.L., Wang, D.Z., Harris, T.M., et al. Modulation of cardiac growth and development by HOP, an unusual homeodomain protein. Cell 110 (2002), 725–735.
61. Stankunas, K., Berger, J., Ruse, C., Sinclair, D.A., Randazzo, F., Brock, H.W., The enhancer of polycomb gene of Drosophila encodes a chromatin protein conserved in yeast and mammals. Development 125 (1998), 4055–4066.
62. Takeda, N., Jain, R., Leboeuf, M.R., Padmanabhan, A., Wang, Q., Li, L., et al. Hopx expression defines a subset of multipotent hair follicle stem cells and a progenitor population primed to give rise to K6+ niche cells. Development 140 (2013), 1655–1664.
63. Takeda, N., Jain, R., LeBoeuf, M.R., Wang, Q., Lu, M.M., Epstein, J.A., Interconversion between intestinal stem cell populations in distinct niches. Science 334 (2011), 1420–1424.
64. Trelsman, J., Gönczy, P., Vashishtha, M., Harris, E., Desplan, C., A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell 59 (1989), 553–562.
65. Trivedi, C.M., Cappola, T.P., Margulies, K.B., Epstein, J.A., Homeodomain only protein x is down-regulated in human heart failure. J Mol Cell Cardiol 50 (2011), 1056–1058.
66. Trivedi, C.M., Zhu, W., Wang, Q., Jia, C., Kee, H.J., Li, L., et al. Hopx and Hdac2 interact to modulate Gata4 acetylation and embryonic cardiac myocyte proliferation. Dev Cell 19 (2010), 450–459.
67. Vasiliev, O., Rhodes, S.J., Beebe, D.C., Identification and expression of Hop, an atypical homeobox gene expressed late in lens fiber cell terminal differentiation. Mol Vis 13 (2007), 114–124.
68. Waraya, M., Yamashita, K., Katoh, H., Ooki, A., Kawamata, H., Nishimiya, H., et al. Cancer specific promoter CpG Islands hypermethylation of HOP homeobox (HOPX) gene and its potential tumor suppressive role in pancreatic carcinogenesis. BMC Cancer, 12, 2012, 397.
69. Weidenfeld, J., Shu, W., Zhang, L., Millar, S.E., Morrisey, E.E., The WNT7b promoter is regulated by TTF-1, GATA6, and Foxa2 in lung epithelium. J Biol Chem 277 (2002), 21061–21070.
70. Yamaguchi, S., Asanoma, K., Takao, T., Kato, K., Wake, N., Homeobox gene HOPX is epigenetically silenced in human uterine endometrial cancer and suppresses estrogen-stimulated proliferation of cancer cells by inhibiting serum response factor. Int J Cancer 124 (2009), 2577–2588.
71. Yamashita, K., Katoh, H., Watanabe, M., The homeobox only protein homeobox (HOPX) and colorectal cancer. Int J Mol Sci 14 (2013), 23231–23243.
72. Yamashita, K., Kim, M.S., Park, H.L., Tokumaru, Y., Osada, M., Inoue, H., et al. HOP/OB1/NECC1 promoter DNA is frequently hypermethylated and involved in tumorigenic ability in esophageal squamous cell carcinoma. Mol Cancer Res 6 (2008), 31–41.
73. Yang, J.M., Sim, S.M., Kim, H.Y., Park, G.T., Expression of the homeobox gene, HOPX, is modulated by cell differentiation in human keratinocytes and is involved in the expression of differentiation markers. Eur J Cell Biol 89 (2010), 537–546.
74. Yin, Z., Gonzales, L., Kolla, V., Rath, N., Zhang, Y., Lu, M.M., et al. Hop functions downstream of Nkx2.1 and GATA6 to mediate HDAC-dependent negative regulation of pulmonary gene expression. Am J Physiol Lung Cell Mol Physiol 291 (2006), L191–L199.
75. Zhong, Y.F., Butts, T., Holland, P.W., HomeoDB: a database of homeobox gene diversity. Evol Dev 10 (2008), 516–518.