CUX1 transcription factors: From biochemical activities and cell-based assays to mouse models and human diseases

Gene

Volumn 497, Issue 1, 2012, Pages 18-26

  Hulea, Laura ^a,b   Nepveu, Alain ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Cancer; Cell cycle; Genomic instability; Kidney diseases; Neurological disorders; Obesity

Indexed keywords

CATHEPSIN L; LEPTIN RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CUX1; UNCLASSIFIED DRUG;

ACUTE LEUKEMIA; APOPTOSIS; BONE DEVELOPMENT; BRAIN DEVELOPMENT; BREAST CANCER; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; COGNITIVE DEFECT; DENDRITE; DNA BINDING; DNA REPLICATION; DNA SEQUENCE; FIBROSING ALVEOLITIS; GENE EXPRESSION; GENOMIC INSTABILITY; GLOMERULOSCLEROSIS; HUMAN; KIDNEY DEVELOPMENT; KIDNEY DISEASE; KIDNEY POLYCYSTIC DISEASE; LIVER CELL CARCINOMA; LIVER DEVELOPMENT; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; MYELOPROLIFERATIVE DISORDER; NERVE DEGENERATION; NERVE FIBER GROWTH; NONHUMAN; OBESITY; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SPINE; SYNAPSE;

ANIMALS; CELL CYCLE; CELL MOVEMENT; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; KIDNEY DISEASES; MICE; MICE, TRANSGENIC; NEOPLASM INVASIVENESS; NEOPLASMS; NERVOUS SYSTEM DISEASES; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRESSOR PROTEINS;

MUS MUSCULUS;

EID: 84857798294     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2012.01.039     Document Type: Review

References (100)

1. Ai W., Toussaint E., Roman A. CCAAT displacement protein binds to and negatively regulates human papillomavirus type 6 E6, E7, and E1 promoters. J. Virol. 1999, 73:4220-4229.
2. Alcalay N.I., Vanden Heuvel G.B. Regulation of cell proliferation and differentiation in the kidney. Front. Biosci. 2009, 14:4978-4991.
3. Alcalay N.I., Brantley J.G., Sharma M., Gooch J.L., Vanden Heuvel G.B. Ectopic expression of the homeobox gene Cux-1 rescues calcineurin inhibition in mouse embryonic kidney cultures. Dev. Dyn. 2007, 236:184-191.
4. Alcalay N.I., et al. Acceleration of polycystic kidney disease progression in cpk mice carrying a deletion in the homeodomain protein Cux1. Am. J. Physiol. Renal Physiol. 2008, 295:F1725-F1734.
5. Aleksic T., et al. CUTL1 promotes tumor cell migration by decreasing proteasome-mediated Src degradation. Oncogene 2007, 26:5939-5949.
6. Amiri K.I., Ha H.C., Smulson M.E., Richmond A. Differential regulation of CXC ligand 1 transcription in melanoma cell lines by poly (ADP-ribose) polymerase-1. Oncogene 2006, 25:7714-7722.
7. Bafico A., Liu G., Goldin L., Harris V., Aaronson S.A. An autocrine mechanism for constitutive Wnt pathway activation in human cancer cells. Cancer Cell 2004, 6:497-506.
8. Barberis A., Superti-Furga G., Busslinger M. Mutually exclusive interaction of the CCAAT-binding factor and of a displacement protein with overlapping sequences of a histone gene promoter. Cell 1987, 50:347-359.
9. Blanc R. The production of wing scalloping in Drosophila melanogaster. Univ. Calif. Publ. Zool. 1942, 49:1-31.
10. Blochlinger K., Bodmer R., Jan L.Y., Jan Y.N. Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 1990, 4:1322-1331.
11. Bodmer R., Barbel S., Shepherd S., Jack J.W., Jan L.Y., Jan Y.N. Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 1987, 51:293-307.
12. Brantley J.G., Sharma M., Alcalay N.I., Heuvel G.B.V. Cux-1 transgenic mice develop glomerulosclerosis and interstitial fibrosis. Kidney Int. 2003, 63:1240-1248.
13. Cadieux C., Fournier S., Peterson A.C., Bedard C., Bedell B.J., Nepveu A. Transgenic mice expressing the p75 CCAAT-displacement protein/Cut homeobox isoform develop a myeloproliferative disease-like myeloid leukemia. Cancer Res. 2006, 66:9492-9501.
14. Cadieux C., et al. Polycystic kidneys caused by sustained expression of Cux1 isoform p75. J. Biol. Chem. 2008, 283:13817-13824.
15. Cadieux C., et al. Mouse mammary tumor virus p75 and p110 CUX1 transgenic mice develop mammary tumors of various histologic types. Cancer Res. 2009, 69:7188-7197.
16. Cardenas-Rodriguez M., Badano J. Ciliary biology: understanding the cellular and genetic basis of human ciliopathies. Am. J. Med. Genet. C Semin. Med. Genet. 2009, 151C:263-280.
17. Ceru S., et al. Stefin B interacts with histones and cathepsin L in the nucleus. J. Biol. Chem. 2010, 285:10078-10086.
18. Chapman H.A. Cathepsins as transcriptional activators?. Dev. Cell 2004, 6:610-611.
19. Coqueret O., Berube G., Nepveu A. The mammalian Cut homeodomain protein functions as a cell-cycle-dependent transcriptional repressor which downmodulates p21WAF1/CIP1/SDI1 in S phase. EMBO J. 1998, 17:4680-4694.
20. Cubelos B., Nieto M. Intrinsic programs regulating dendrites and synapses in the upper layer neurons of the cortex. Communicative Integr. Biol. 2010, 3:483-486.
21. Cubelos B., et al. Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 2010, 66:523-535.
22. De Vos J., et al. Comparison of gene expression profiling between malignant and normal plasma cells with oligonucleotide arrays. Oncogene 2002, 21:6848-6857.
23. Denhardt D.T., et al. Close relationship of the major excreted protein of transformed murine fibroblasts to thiol-dependent cathepsins. Cancer Res. 1986, 46:4590-4593.
24. Fisher B., et al. Treatment of lymph-node-negative, oestrogen-receptor-positive breast cancer: long-term findings from National Surgical Adjuvant Breast and Bowel Project randomised clinical trials. Lancet 2004, 364:858-868.
25. Ganem N.J., Godinho S.A., Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009, 460:278-282.
26. Gooch J.L., Toro J.J., Guler R.L., Barnes J.L. Calcineurin A-alpha but not A-beta is required for normal kidney development and function. Am. J. Pathol. 2004, 165:1755-1765.
27. Gottesman M.M., Sobel M.E. Tumor promoters and Kirsten sarcoma virus increase synthesis of a secreted glycoprotein by regulating levels of translatable mRNA. Cell 1980, 19:449-455.
28. Goulet B., Nepveu A. Complete and limited proteolysis in cell cycle progression. Cell Cycle 2004, 3:986-989.
29. Goulet B., et al. Characterization of a tissue-specific CDP/Cux isoform, p75, activated in breast tumor cells. Cancer Res. 2002, 62:6625-6633.
30. Goulet B., et al. A cathepsin L isoform that is devoid of a signal peptide localizes to the nucleus in S phase and processes the CDP/Cux transcription factor. Mol. Cell 2004, 14:207-219.
31. Goulet B., et al. Increased expression and activity of nuclear cathepsin L in cancer cells suggests a novel mechanism of cell transformation. Mol. Cancer Res. 2007, 5:899-907.
32. Grueber W.B., Jan L.Y., Jan Y.N. Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 2003, 112:805-818.
33. Harada R., et al. Genome-wide location analysis and expression studies reveal a role for p110 CUX1 in the activation of DNA replication genes. Nucleic Acids Res. 2008, 36:189-202.
34. Hertweck H. Anatomie und variabilitaet des nerven-systems und der sinneorgane von Drosophila melanogaster. J. Exp. Zool. 1931, 139:559-663.
35. Heuvel G.B.V., Bodmer R., McConnell K.R., Nagami G.T., Igarashi P. Expression of a Cut-related homeobox gene in developing and polycystic mouse kidney. Kidney Int. 1996, 50:453-461.
36. Hilmi C., et al. IGF1 promotes resistance to apoptosis in melanoma cells through an increased expression of BCL2, BCL-X(L), and survivin. J. Investig. Dermatol. 2008, 128:1499-1505.
37. Hou X., et al. Cystin, a novel cilia-associated protein, is disrupted in the cpk mouse model of polycystic kidney disease. J. Clin. Invest. 2002, 109:533-540.
38. Jinushi-Nakao S., Arvind R., Amikura R., Kinameri E., Liu A.W., Moore A.W. Knot/Collier and cut control different aspects of dendrite cytoskeleton and synergize to define final arbor shape. Neuron 2007, 56:963-978.
39. Kedinger V., Nepveu A. The roles of CUX1 homeodomain proteins in the establishment of a transcriptional program required for cell migration and invasion. Cell Adh. Migr. 2010, 4:348-352.
40. Kedinger V., et al. p110 CUX1 homeodomain protein stimulates cell migration and invasion in part through a regulatory cascade culminating in the repression of E-cadherin and occludin. J. Biol. Chem. 2009, 284:27701-27711.
41. Kojima K., et al. MicroRNA122 is a key regulator of alpha-fetoprotein expression and influences the aggressiveness of hepatocellular carcinoma. Nat. Commun. 2011, 2:338.
42. Komiyama T., Luo L. Intrinsic control of precise dendritic targeting by an ensemble of transcription factors. Curr. Biol. 2007, 17:278-285.
43. Kwon M., Godinho S.A., Chandhok N.S., Ganem N.J., Azioune A., Thery M., Pellman D. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 2008, 22:2189-2203.
44. Lafreniere R.G., et al. Unstable insertion in the 5' flanking region of the cystatin B gene is the most common mutation in progressive myoclonus epilepsy type 1, EPM1. Nat. Genet. 1997, 15:298-302.
45. Ledford A.W., et al. Deregulated expression of the homeobox gene Cux-1 in transgenic mice results in downregulation of p27 (kip1) expression during nephrogenesis, glomerular abnormalities, and multiorgan hyperplasia. Dev. Biol. 2002, 245:157-171.
46. Li Y., et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:15853-15858.
47. Li N., Zhao C.-T., Wang Y., Yuan X.-B. The transcription factor Cux1 regulates dendritic morphology of cortical pyramidal neurons. PLoS One 2010, 5:e10596. (Electronic Resource).
48. Lin T.P., Guzman R.C., Osborn R.C., Thordarson G., Nandi S. Role of endocrine, autocrine, and paracrine interactions in the development of mammary hyperplasia in Wnt-1 transgenic mice. Cancer Res. 1992, 52:4413-4419.
49. Luo J., Solimini N.L., Elledge S.J. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 2009, 136:823-837.
50. Maitra U., Seo J., Lozano M.M., Dudley J.P. Differentiation-induced cleavage of Cutl1/CDP generates a novel dominant-negative isoform that regulates mammary gene expression. Mol. Cell. Biol. 2006, 26:7466-7478.
51. Marshall W.F. Basal bodies platforms for building cilia. Curr. Top. Dev. Biol. 2008, 85:1-22.
52. Michl P., Downward J. CUTL1: a key mediator of TGFbeta-induced tumor invasion. Cell Cycle 2006, 5:132-134.
53. Michl P., et al. CUTL1 is a target of TGF (beta) signaling that enhances cancer cell motility and invasiveness. Cancer Cell 2005, 7:521-532.
54. Miyoshi K., et al. Activation of different Wnt/beta-catenin signaling components in mammary epithelium induces transdifferentiation and the formation of pilar tumors. Oncogene 2002, 21:5548-5556.
55. Moon N.S., Berube G., Nepveu A. CCAAT displacement activity involves Cut repeats 1 and 2, not the Cut homeodomain. J. Biol. Chem. 2000, 275:31325-31334.
56. Moon N.S., Premdas P., Truscott M., Leduy L., Berube G., Nepveu A. S phase-specific proteolytic cleavage is required to activate stable DNA binding by the CDP/Cut homeodomain protein. Mol. Cell. Biol. 2001, 21:6332-6345.
57. Moon N.S., Rong Zeng W., Premdas P., Santaguida M., Berube G., Nepveu A. Expression of N-terminally truncated isoforms of CDP/CUX is increased in human uterine leiomyomas. Int. J. Cancer 2002, 100:429-432.
58. Moore A.W. Intrinsic mechanisms to define neuron class-specific dendrite arbor morphology. Cell Adh. Migr. 2008, 2:81-82.
59. Mrozek E., Shapiro C.L. Survivorship and complications of treatment in breast cancer. Clin. Adv. Hematol. Oncol. 2005, 3:211-222. 238.
60. Nepveu A. Role of the multifunctional CDP/Cut/Cux homeodomain transcription factor in regulating differentiation, cell growth and development. Gene 2001, 270:1-15.
61. Neufeld E.J., Skalnik D.G., Lievens P.M., Orkin S.H. Human CCAAT displacement protein is homologous to the Drosophila homeoprotein, cut. Nat. Genet. 1992, 1:50-55.
62. Nieto M., et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J. Comp. Neurol. 2004, 479:168-180.
63. Ochiai E., et al. CDP/cut is an osteoblastic coactivator of the vitamin D receptor (VDR). J. Bone Miner. Res. 2010, 25:1157-1166.
64. Ong A.C., Wheatley D.N. Polycystic kidney disease-the ciliary connection. Lancet 2003, 361:774-776.
65. Ripka S., et al. WNT5A-target of CUTL1 and potent modulator of tumor cell migration and invasion in pancreatic cancer. Carcinogenesis 2007, 28:1178-1187.
66. Ripka S., et al. CUX1: target of Akt signalling and mediator of resistance to apoptosis in pancreatic cancer. Gut 2010, 59:1101-1110.
67. Ripka S., et al. Glutamate receptor GRIA3-target of CUX1 and mediator of tumor progression in pancreatic cancer. Neoplasia 2010, 12:659-667.
68. Rowell J.J., Mallik A.K., Dugas-Ford J., Ragsdale C.W. Molecular analysis of neocortical layer structure in the ferret. J. Comp. Neurol. 2010, 518:3272-3289.
69. Saito T., et al. Neocortical layer formation of human developing brains and lissencephalies: consideration of layer-specific marker expression. Cereb. Cortex 2011, 21:588-596.
70. Sansregret L., Nepveu A. The multiple roles of CUX1: insights from mouse models and cell-based assays. Gene 2008, 412:84-94.
71. Sansregret L., Nepveu A. Gene signatures of genomic instability as prognostic tools for breast cancer. Future Oncol. 2011, 7:591-594.
72. Sansregret L., et al. The p110 isoform of the CDP/Cux transcription factor accelerates entry into S phase. Mol. Cell. Biol. 2006, 26:2441-2455.
73. Sansregret L., Gallo D., Santaguida M., Leduy L., Harada R., Nepveu A. Hyperphosphorylation by cyclin B/CDK1 in mitosis resets CUX1 DNA binding clock at each cell cycle. J. Biol. Chem. 2010, 285:32834-32843.
74. Sansregret L., et al. Cut homeobox 1 causes chromosomal instability by promoting bipolar division after cytokinesis failure. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1949-1954.
75. Santaguida M., Ding Q., Berube G., Truscott M., Whyte P., Nepveu A. Phosphorylation of the CCAAT displacement protein (CDP)/Cux transcription factor by cyclin A-Cdk1 modulates its DNA binding activity in G(2). J. Biol. Chem. 2001, 276:45780-45790.
76. Schlange T., Matsuda Y., Lienhard S., Huber A., Hynes N.E. Autocrine WNT signaling contributes to breast cancer cell proliferation via the canonical WNT pathway and EGFR transactivation. Breast Cancer Res. 2007, 9.
77. Seguin L., et al. CUX1 and E2F1 regulate coordinated expression of the mitotic complex genes Ect2, MgcRacGAP, and MKLP1 in S phase. Mol. Cell. Biol. 2009, 29:570-581.
78. Sekharam M., et al. Insulin-like growth factor 1 receptor enhances invasion and induces resistance to apoptosis of colon cancer cells through the Akt/Bcl-x(L) pathway. Cancer Res. 2003, 63:7708-7716.
79. Siam R., Harada R., Cadieux C., Battat R., Vadnais C., Nepveu A. Transcriptional activation of the Lats1 tumor suppressor gene in tumors of CUX1 transgenic mice. Mol. Cancer 2009, 8:60-70.
80. Skalnik D.G. Transcriptional mechanisms regulating myeloid-specific genes. Gene 2002, 284:1-21.
81. Skalnik D.G., Strauss E.C., Orkin S.H. CCAAT displacement protein as a repressor of the myelomonocytic-specific gp91-phox gene promoter. J. Biol. Chem. 1991, 266:16736-16744.
82. Stratigopoulos G., et al. Regulation of Fto/Ftm gene expression in mice and humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R1185-R1196.
83. Stratigopoulos G., LeDuc C.A., Cremona M.L., Chung W.K., Leibel R.L. Cut-like homeobox 1 (CUX1) regulates expression of the fat mass and obesity-associated and retinitis pigmentosa GTPase regulator-interacting protein-1-like (RPGRIP1L) genes and coordinates leptin receptor signaling. J. Biol. Chem. 2011, 286:2155-2170.
84. Thoennissen N.H., Lasho T., Thoennissen G.B., Ogawa S., Tefferi A., Koeffler H.P. Novel CUX1 missense mutation in association with 7q- at leukemic transformation of MPN. Am. J. Hematol. 2011, 86:703-705.
85. Thomas V., Samanta S., Fikrig E. Anaplasma phagocytophilum increases cathepsin L activity, thereby globally influencing neutrophil function. Infect. Immun. 2008, 76:4905-4912.
86. Thompson S.L., Compton D.A. Examining the link between chromosomal instability and aneuploidy in human cells. J. Cell Biol. 2008, 180:665-672.
87. Truscott M., et al. CDP/Cux stimulates transcription from the DNA polymerase alpha gene promoter. Mol. Cell. Biol. 2003, 23:3013-3028.
88. Truscott M., Denault J.B., Goulet B., Leduy L., Salvesen G.S., Nepveu A. Carboxyl-terminal proteolytic processing of CUX1 by a caspase enables transcriptional activation in proliferating cells. J. Biol. Chem. 2007, 282:30216-30226.
89. Truscott M., Harada R., Vadnais C., Robert F., Nepveu A. p110 CUX1 cooperates with E2F transcription factors in the transcriptional activation of cell cycle-regulated genes. Mol. Cell. Biol. 2008, 28:3127-3138.
90. Tsutsumi S., et al. Two distinct gene expression signatures in pediatric acute lymphoblastic leukemia with MLL rearrangements. Cancer Res. 2003, 63:4882-4887.
91. Tufarelli C., Fujiwara Y., Zappulla D.C., Neufeld E.J. Hair defects and pup loss in mice with targeted deletion of the first cut repeat domain of the Cux/CDP homeoprotein gene. Dev. Biol. 1998, 200:69-81.
92. Ueda Y., Su Y., Richmond A. CCAAT displacement protein regulates nuclear factor-kappa beta-mediated chemokine transcription in melanoma cells. Melanoma Res. 2007, 17:91-103.
93. Uyttendaele H., Soriano J.V., Montesano R., Kitajewski J. Notch4 and Wnt-1 proteins function to regulate branching morphogenesis of mammary epithelial cells in an opposing fashion. Dev. Biol. 1998, 196:204-217.
94. Vanden Heuvel G.B., et al. Hepatomegaly in transgenic mice expressing the homeobox gene Cux-1. Mol. Carcinog. 2005, 43:18-30.
95. Vandenheuvel G.B., Quaggin S.E., Igarashi P. A unique variant of a homeobox gene related to Drosophila Cut is expressed in mouse testis. Biol. Reprod. 1996, 55:731-739.
96. Vierkotten J., Dildrop R., Peters T., Wang B., R√other U. Ftm is a novel basal body protein of cilia involved in Shh signalling. Dev. (Cambridge, England) 2007, 134:2569-2577.
97. Voduc K.D., Cheang M.C., Tyldesley S., Gelmon K., Nielsen T.O., Kennecke H. Breast cancer subtypes and the risk of local and regional relapse. J. Clin. Oncol. 2010, 28:1684-1691.
98. Wilson B.J., Harada R., LeDuy L., Hollenberg M.D., Nepveu A. CUX1 transcription factor is a downstream effector of the proteinase-activated receptor 2 (PAR2). J. Biol. Chem. 2009, 284:36-45.
99. Xu H., et al. Liver-enriched transcription factors regulate microRNA-122 that targets CUTL1 during liver development. Hepatology 2010, 52:1431-1442.
100. Yoder B.K., Hou X., Guay-Woodford L.M. The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. Journal of the American Society of Nephrology: JASN 2002, 13:2508-2516.