*165160
V-JUN AVIAN SARCOMA VIRUS 17 ONCOGENE HOMOLOG; JUN

Alternative titles; symbols
ONCOGENE JUN

Other entities represented in this entry:
ACTIVATOR PROTEIN 1, INCLUDED; AP1, INCLUDED
ENHANCER-BINDING PROTEIN AP1, INCLUDED

HGNC Approved Gene Symbol: JUN

Cytogenetic location: 1p32.1     Genomic coordinates (GRCh37): 1:59,246,462 - 59,249,784 (from NCBI)

TEXT
Description
The oncogene JUN is the putative transforming gene of avian sarcoma virus 17; it appears to be derived from a gene of the chicken genome and has homologs in several other vertebrate species. (The name JUN comes from the Japanese 'ju-nana,' meaning the number 17.) JUN was originally thought to be identical to the transcription factor AP1. However, it is now known that AP1 is not a single protein, but constitutes a group of related dimeric basic region-leucine zipper proteins that belong to the JUN, FOS (164810), MAF (177075), and ATF (see 603148) subfamilies. The various dimers recognize either 12-O-tetradecanoylphorbol-13-acetate (TPA) response elements or cAMP response elements. JUN is the most potent transcriptional activator in its group, and its transcriptional activity is attenuated and sometimes antagonized by JUNB (165161). For a review of the structure and function of the AP1 transcription complexes, see Shaulian and Karin (2002).

Cloning
Bohmann et al. (1987) isolated the human protooncogene JUN and found that the deduced amino acid sequence is more than 80% identical to that of the viral protein. Expression of cloned cDNA in bacteria produced a protein with sequence-specific DNA-binding properties identical to the phorbol ester-inducible enhancer-binding protein AP1. Antibodies raised against 2 distinct peptides derived from JUN reacted specifically with human AP1. In addition, partial amino acid sequence of purified AP1 revealed tryptic peptides in common with the JUN protein. Nucleotide sequence analysis indicated that the COOH-terminus of JUN is similar to the corresponding part of a yeast transcriptional activator.

Hattori et al. (1988) isolated a genomic clone of human JUN and determined its primary structure and transcription pattern. Transfection experiments showed that the cloned gene is functional, as it encodes a trans-acting factor that stimulates transcription of an AP1-dependent reporter gene.

Gene Function
Lamph et al. (1988) investigated regulation of murine c-jun gene transcription and found that both serum and phorbol-ester TPA induced c-jun gene expression.

Marx (1988) reviewed information indicating that the protein encoded by the JUN gene acts directly to activate gene transcription in response to cell stimulation; that the product of the FOS oncogene cooperates with the JUN product in fostering gene transcription; that there is a structural and functional similarity between JUN and GCN4, which induces the activity of a large set of genes needed for amino acid synthesis in yeast; that specifically both have a DNA-binding domain on the carboxyl end essential for the activation of genes; that the JUN and FOS proteins are held together in a complex by a leucine zipper; and that there are other JUN genes in addition to the original one.

Shaulian et al. (2000) found that in mouse fibroblasts, Jun was necessary for cell cycle reentry of ultraviolet (UV)-irradiated cells but did not participate in the response to ionizing radiation. Cells lacking Jun underwent prolonged cell cycle arrest but resisted apoptosis, whereas cells that expressed Jun constitutively did not arrest and undergo apoptosis. This function of Jun was exerted through negative regulation of p53 (191170) association with the p21 (116899) promoter. Cells lacking Jun exhibited prolonged p21 induction, whereas constitutive Jun inhibited UV-mediated p21 induction.

Whitfield et al. (2001) noted that apoptosis induced in rat sympathetic neurons by nerve growth factor (NGF; see 162030) withdrawal can be blocked by inhibitors of RNA and protein synthesis. They presented experimental evidence that activation of the JNK (see 601158)/JUN pathway and increased expression of BIM (603827) are key events required for cytochrome c release and apoptosis following NGF withdrawal.

Sphingosylphosphocholine (SPC) is a deacylated derivative of sphingomyelin known to accumulate in Niemann-Pick disease type A (257200). SPC is a potent mitogen that increases intracellular free Ca(2+) and free arachidonate through pathways that are only partly protein kinase C-dependent. Berger et al. (1995) showed that SPC increases specific DNA-binding activity of transcription activator AP1 in electrophoretic mobility-shift assays.

Using a Drosophila model synapse, Sanyal et al. (2002) analyzed cellular functions and regulation of the immediate-early transcription factor AP1, a heterodimer of the basic leucine zipper proteins FOS and JUN. They observed that AP1 positively regulates synaptic strength and synapse number, thus showing a greater range of influence than CREB (123810). Observations from genetic epistasis and RNA quantification experiments indicate that AP1 acts upstream of CREB, regulates levels of CREB mRNA, and functions at the top of the hierarchy of transcription factors known to regulate long-term plasticity. A JUN-kinase signaling module provided a CREB-independent route for neuronal AP1 activation; thus, CREB regulation of AP1 expression may, in some neurons, constitute a positive feedback loop rather than the primary step in AP1 activation.

Mathas et al. (2002) found AP1 constitutively activated, with robust JUN and JUNB overexpression, in all cell lines derived from patients with classical Hodgkin lymphoma (236000) and anaplastic large cell lymphoma (ALCL), but not in other lymphoma types. AP1 supported proliferation of Hodgkin cells, but suppressed apoptosis of ALCL cells. Mathas et al. (2002) noted that, whereas JUN is upregulated by an autoregulatory process, JUNB is under the control of nuclear factor kappa-B (NFKB; 164011). They found that AP1 and NFKB cooperate and stimulate expression of the cell cycle regulator cyclin D2 (123833), the protooncogene MET (164860), and the lymphocyte homing receptor CCR7 (600242), which are all strongly expressed in primary Hodgkin/Reed-Sternberg (HRS) cells.

Wertz et al. (2004) reported that human DET1 (608727) promotes ubiquitination and degradation of the protooncogenic transcription factor c-Jun by assembling a multisubunit ubiquitin ligase containing DNA damage-binding protein-1 (DDB1; 600045), cullin 4A (CUL4A; 603137), regulator of cullins-1 (ROC1; 603814), and constitutively photomorphogenic-1 (COP1; 608067). Ablation of any subunit by RNA interference stabilized c-Jun and increased c-Jun-activated transcription. Wertz et al. (2004) concluded that their findings characterized a c-Jun ubiquitin ligase and define a specific function for DET1 in mammalian cells.

JUN and N-terminal kinases (JNK) are essential for neuronal microtubule assembly and apoptosis. Phosphorylation of the activating protein 1 (AP1) transcription factor c-Jun, at multiple sites within its transactivation domain, is required for JNK-induced neurotoxicity. Nateri et al. (2004) reported that in neurons the stability of c-Jun is regulated by the E3 ligase SCF(Fbw7) (FBXW7; 606278), which ubiquitinates phosphorylated c-Jun and facilitates c-Jun degradation. Fbxw7 depletion resulted in accumulation of phosphorylated c-Jun, stimulation of AP1 activity, and neuronal apoptosis. SCF-7 therefore antagonizes the apoptotic c-Jun-dependent effector arm of JNK signaling, allowing neurons to tolerate potentially neurotoxic JNK activity.

Fang and Kerppola (2004) found evidence that JUN proteins ubiquitinated by ITCH (606409) are targeted to lysosomes for degradation. Mutation of the ITCH recognition motif in the N terminus of JUN eliminated its ubiquitination and increased its stability.

Ikeda et al. (2004) generated transgenic mice expressing dominant-negative c-Jun specifically in the osteoclast lineage and found that they developed severe osteopetrosis due to impaired osteoclastogenesis. Blockade of c-Jun signaling also markedly inhibited soluble RANKL (602642)-induced osteoclast differentiation in vitro. Overexpression of nuclear factor of activated T cells 1 (NFATC2; 600490) or NFATC1 (600489) promoted differentiation of osteoclast precursor cells into tartrate-resistant acid phosphatase-positive (TRAP-positive) multinucleated osteoclast-like cells even in the absence of RANKL. These osteoclastogenic activities of NFAT were abrogated by overexpression of dominant-negative c-Jun. Ikeda et al. (2004) concluded that c-Jun signaling in cooperation with NFAT is crucial for RANKL-regulated osteoclast differentiation.

Gao et al. (2004) found in the case of c-JUN and JUNB that extracellular stimuli modulate protein turnover by regulating the activity of an E3 ligase by means of its phosphorylation. Activation of the Jun amino-terminal kinase (JNK; see 601158) mitogen-activated protein kinase (MAPK) cascade after T cell stimulation accelerated degradation of c-JUN and JUNB through phosphorylation-dependent activation of the E3 ligase ITCH. Gao et al. (2004) found that this pathway modulates cytokine production by effector T cells.

Nateri et al. (2005) showed that phosphorylated c-JUN interacts with the HMG-box transcription factor TCF4 (TCF7L2; 602228) to form a ternary complex containing c-JUN, TCF4, and beta-catenin (see 116806). Chromatin immunoprecipitation assays revealed JNK-dependent c-JUN-TCF4 interaction on the c-JUN promoter, and c-JUN and TCF4 cooperatively activated the c-JUN promoter in reporter assays in a beta-catenin-dependent manner. In the Apc(Min) mouse model of intestinal cancer (see 611731), genetic abrogation of c-JUN N-terminal phosphorylation or gut-specific conditional c-JUN inactivation reduced tumor number and size and prolonged life span. Therefore, Nateri et al. (2005) concluded that the phosphorylation-dependent interaction between c-JUN and TCF4 regulates intestinal tumorigenesis by integrating JNK and APC/beta-catenin, 2 distinct pathways activating WNT signaling.

Koyama-Nasu et al. (2007) showed that FBL10 (FBXL10; 609078) interacted with JUN and repressed JUN-mediated transcription in human cell lines. Chromatin immunoprecipitation assays demonstrated that FBL10 was present at the JUN promoter and that JUN was required for recruitment of FBL10. FBL10 bound unmethylated CpG sequences in the JUN promoter through its CxxC zinc finger and tethered transcriptional repressor complexes. Suppression of FBL10 expression by RNA interference induced transcription of JUN and JUN target genes and caused aberrant cell cycle progression and increased UV-induced cell death. Furthermore, FBL10 protein and mRNA were downregulated in response to UV in an inverse correlation with JUN. Koyama-Nasu et al. (2007) concluded that FBL10 is a key regulator of JUN function.

Aguilera et al. (2011) demonstrated that unphosphorylated, but not N-terminally phosphorylated, c-Jun interacts with MBD3 (603573) and thereby recruits the nucleosome remodeling and histone acetylation (NuRD) repressor complex. MBD3 depletion in colon cancer cells increased histone acetylation at AP1-dependent promoters, which resulted in increased target gene expression. The intestinal stem cell marker LGR5 (606667) was identified as a novel target gene controlled by c-Jun/MBD3. Gut-specific conditional deletion of Mbd3 in mice stimulated c-Jun activity and increased progenitor cell proliferation. In response to inflammation, Mbd3 deficiency resulted in colonic hyperproliferation, and Mbd3 gut-null mice showed markedly increased susceptibility to colitis-induced tumorigenesis. Aguilera et al. (2011) noted that concomitant inactivation of a single allele of c-Jun reverted physiologic and pathologic hyperproliferation, as well as the increased tumorigenesis in Mbd3 gut-null mice. Thus, the transactivation domain of c-Jun recruits MBD3/NuRD to AP1 target genes to mediate gene repression, and this repression is relieved by JNK (601158)-mediated c-Jun N-terminal phosphorylation.

Gene Structure
Hattori et al. (1988) determined that the JUN gene has no introns.

Mapping
Haluska et al. (1988) isolated a genomic DNA clone encompassing the JUN gene and used it to determine the chromosomal location. Southern blot analysis of a rodent-human somatic cell hybrid panel indicated that JUN is situated on 1p. In situ hybridization narrowed the assignment to 1p32-p31, a chromosomal region involved in both translocations and deletions in human malignancies. By in situ hybridization, Hattori et al. (1988) mapped JUN to 1p32-p31.

Mattei et al. (1990) mapped the mouse homolog to chromosome 4. Bahary et al. (1991) presented molecular genetic linkage maps of mouse chromosome 4 which established the breakpoints in the mouse 4/human 1p region of homology to a 2-cM interval between Ifa and Jun in mouse and to the interval between JUN and ACADM (607008) in the human.

Animal Model
Hilberg et al. (1993) developed Jun-null mice by gene targeting. Heterozygous mutant mice appeared normal, but embryos lacking Jun died between midgestation and late gestation and exhibited impaired hepatogenesis, altered fetal liver erythropoiesis, and generalized edema. Jun-defective embryonic stem cells were able to participate in the development of all somatic cells in chimeric mice except liver cells, indicating an essential function of Jun in hepatogenesis.

By alanine substitution of ser63 and ser73 of mouse Jun, Behrens et al. (1999) demonstrated that phosphorylation on these residues was required for several apoptotic functions. Mouse fibroblasts carrying mutated Jun had proliferation- and stress-induced apoptotic defects accompanied by reduced AP1 activity. Mutant mice were smaller than controls, and they were resistant to epileptic seizures and neuronal apoptosis induced by the excitotoxic amino acid kainate. Primary mutant neurons were also protected from apoptosis.

Eferl et al. (2003) used liver-specific inactivation of Jun at different stages of tumor development to study its role in chemically induced hepatocellular carcinomas (HCCs) in mice. The requirement for Jun was restricted to early stages of tumor development, and the number and size of hepatic tumors was dramatically reduced when Jun was inactivated after the tumor had initiated. The impaired tumor development correlated with increased levels of p53 and its target gene Noxa (PMAIP1; 604959), resulting in the induction of apoptosis without affecting cell proliferation. Primary hepatocytes lacking Jun showed increased sensitivity to tumor necrosis factor-alpha (TNF; 191160)-induced apoptosis, which was abrogated in the absence of p53. These data indicated that JUN prevents apoptosis by antagonizing p53 activity, illustrating a mechanism that might contribute to the early stages of human HCC development.

See Also:
Bos et al. (1988)

REFERENCES
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2. Bahary, N., Zorich, G., Pachter, J. E., Leibel, R. L., Friedman, J. M. Molecular genetic linkage maps of mouse chromosomes 4 and 6. Genomics 11: 33-47, 1991. [PubMed: 1684952, related citations] [Full Text: Elsevier Science, Pubget]

3. Behrens, A., Sibilia, M., Wagner, E. F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nature Genet. 21: 326-329, 1999. [PubMed: 10080190, related citations] [Full Text: Nature Publishing Group, Pubget]

4. Berger, A., Rosenthal, D., Spiegel, S. Sphingosylphosphocholine, a signaling molecule which accumulates in Niemann-Pick disease type A, stimulates DNA-binding activity of the transcription activator protein AP-1. Proc. Nat. Acad. Sci. 92: 5885-5889, 1995. [PubMed: 7597047, related citations] [Full Text: HighWire Press, Pubget]

5. Bohmann, D., Bos, T. J., Admon, A., Nishimura, T., Vogt, P. K., Tjian, R. Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science 238: 1386-1392, 1987. [PubMed: 2825349, related citations] [Full Text: HighWire Press, Pubget]

6. Bos, T. J., Bohmann, D., Tsuchie, H., Tjian, R., Vogt, P. K. v-jun encodes a nuclear protein with enhancer binding properties of AP-1. Cell 52: 705-712, 1988. [PubMed: 2830989, related citations] [Full Text: Elsevier Science, Pubget]

7. Eferl, R., Ricci, R., Kenner, L., Zenz, R., David, J.-P., Rath, M., Wagner, E. F. Liver tumor development: c-Jun antagonizes the proapoptotic activity of p53. Cell 112: 181-192, 2003. [PubMed: 12553907, related citations] [Full Text: Elsevier Science, Pubget]

8. Fang, D., Kerppola, T. K. Ubiquitin-mediated fluorescence complementation reveals that Jun ubiquitinated by Itch/AIP4 is localized to lysosomes. Proc. Nat. Acad. Sci. 101: 14782-14787, 2004. [PubMed: 15469925, related citations] [Full Text: HighWire Press, Pubget]

9. Gao, M., Labuda, T., Xia, Y., Gallagher, E., Fang, D., Liu, Y.-C., Karin, M. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science 306: 271-275, 2004. [PubMed: 15358865, related citations] [Full Text: HighWire Press, Pubget]

10. Haluska, F. G., Huebner, K., Isobe, M., Nishimura, T., Croce, C. M., Vogt, P. K. Localization of the human JUN protooncogene to chromosome region 1p31-32. Proc. Nat. Acad. Sci. 85: 2215-2218, 1988. [PubMed: 3127828, related citations] [Full Text: HighWire Press, Pubget]

11. Hattori, K., Angel, P., Le Beau, M. M., Karin, M. Structure and chromosomal localization of the functional intronless human JUN protooncogene. Proc. Nat. Acad. Sci. 85: 9148-9152, 1988. [PubMed: 3194415, related citations] [Full Text: HighWire Press, Pubget]

12. Hilberg, F., Aguzzi, A., Howells, N., Wagner, E. F. c-Jun is essential for normal mouse development and hepatogenesis. Nature 365: 179-181, 1993. [PubMed: 8371760, related citations] [Full Text: Nature Publishing Group, Pubget]

13. Ikeda, F., Nishimura, R., Matsubara, T., Tanaka, S., Ioune, J., Reddy, S. V., Hata, K., Yamashita, K., Hiraga, T., Watanabe, T., Kukita, T., Yoshioka, K., Rao, A., Yoneda, T. Critical roles of c-Jun signaling in regulation of NFAT family and RANKL-regulated osteoclast differentiation. J. Clin. Invest. 114: 475-484, 2004. [PubMed: 15314684, related citations] [Full Text: Journal of Clinical Investigation, Pubget]

14. Koyama-Nasu, R., David, G., Tanese, N. The F-box protein Fbl10 is a novel transcriptional repressor of c-Jun. Nature Cell Biol. 9: 1074-1080, 2007. [PubMed: 17704768, related citations] [Full Text: Nature Publishing Group, Pubget]

15. Lamph, W. W., Wamsley, P., Sassone-Corsi, P., Verma, I. M. Induction of proto-oncogene JUN/AP-1 by serum and TPA. Nature 334: 629-631, 1988. [PubMed: 2457172, related citations] [Full Text: Nature Publishing Group, Pubget]

16. Marx, J. L. 'Jun' is bustin' out all over. (Research News). Science 242: 1377-1378, 1988. [PubMed: 3201229, related citations] [Full Text: HighWire Press, Pubget]

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18. Mattei, M. G., Simon-Chazottes, D., Hirai, S.-I., Ryseck, R.-P., Galcheva-Gargova, Z., Guenet, J. L., Mattei, J. F., Bravo, R., Yaniv, M. Chromosomal localization of the three members of the jun proto-oncogene family in mouse and man. Oncogene 5: 151-156, 1990. [PubMed: 2108401, related citations] [Full Text: Pubget]

19. Nateri, A. S., Riera-Sans, L., Da Costa, C., Behrens, A. The ubiquitin ligase SCF(Fbw7) antagonizes apoptotic JNK signaling. Science 303: 1374-1378, 2004. [PubMed: 14739463, related citations] [Full Text: HighWire Press, Pubget]

20. Nateri, A. S., Spencer-Dene, B., Behrens, A. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437: 281-285, 2005. [PubMed: 16007074, related citations] [Full Text: Nature Publishing Group, Pubget]

21. Sanyal, S., Sandstrom, D. J., Hoeffer, C. A., Ramaswami, M. AP-1 function upstream of CREB to control synaptic plasticity in Drosophila. Nature 416: 870-874, 2002. [PubMed: 11976688, related citations] [Full Text: Nature Publishing Group, Pubget]

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24. Wertz, I. E., O'Rourke, K. M., Zhang, Z., Dornan, D., Arnott, D., Deshaies, R. J., Dixit, V. M. Human de-etiolated-1 regulates c-Jun by assembling a CUL4A ubiquitin ligase. Science 303: 1371-1374, 2004. [PubMed: 14739464, related citations] [Full Text: HighWire Press, Pubget]

25. Whitfield, J., Neame, S. J., Paquet, L., Bernard, O., Ham, J. Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29: 629-643, 2001. [PubMed: 11301023, related citations] [Full Text: Elsevier Science, Pubget]

Contributors: Ada Hamosh - updated : 1/28/2011
Patricia A. Hartz - updated : 4/30/2008
Ada Hamosh - updated : 6/29/2007
Ada Hamosh - updated : 2/23/2005
Marla J. F. O'Neill - updated : 1/6/2005
Patricia A. Hartz - updated : 11/22/2004
Ada Hamosh - updated : 6/10/2004
Patricia A. Hartz - updated : 7/8/2003
Patricia A. Hartz - updated : 3/25/2003
Stylianos E. Antonarakis - updated : 2/4/2003
Patricia A. Hartz - updated : 10/30/2002
Patricia A. Hartz - updated : 10/4/2002
Ada Hamosh - updated : 5/8/2002
Stylianos E. Antonarakis - updated : 12/18/2000
Creation Date: Victor A. McKusick : 12/23/1987
Edit History: alopez : 02/04/2011
terry : 1/28/2011
mgross : 4/30/2008
wwang : 2/27/2008
ckniffin : 2/5/2008
mgross : 11/14/2007
alopez : 7/2/2007
terry : 6/29/2007
terry : 3/16/2005
alopez : 2/23/2005
carol : 1/7/2005
terry : 1/6/2005
mgross : 11/22/2004
alopez : 6/11/2004
terry : 6/10/2004
mgross : 7/8/2003
mgross : 3/25/2003
mgross : 2/4/2003
mgross : 10/30/2002
mgross : 10/4/2002
mgross : 10/4/2002
carol : 6/20/2002
terry : 6/19/2002
ckniffin : 6/13/2002
alopez : 5/9/2002
terry : 5/8/2002
terry : 12/7/2001
mgross : 12/18/2000
alopez : 11/4/1998
alopez : 10/22/1998
mark : 3/26/1996
mark : 2/15/1996
mark : 7/24/1995
jason : 6/17/1994
supermim : 3/16/1992
carol : 9/6/1991
carol : 10/3/1990
carol : 9/13/1990