Entry - *604299 - ADAPTOR PROTEIN, PHOSPHOTYROSINE INTERACTION, PH DOMAIN, AND LEUCINE ZIPPER-CONTAINING PROTEIN 1; APPL1 - OMIM
 
* 604299

ADAPTOR PROTEIN, PHOSPHOTYROSINE INTERACTION, PH DOMAIN, AND LEUCINE ZIPPER-CONTAINING PROTEIN 1; APPL1


Alternative titles; symbols

ADAPTOR PROTEIN CONTAINING PH DOMAIN, PTB DOMAIN, AND LEUCINE ZIPPER MOTIF 1
APPL
DIP13-ALPHA
AKT2 INTERACTOR


HGNC Approved Gene Symbol: APPL1

Cytogenetic location: 3p14.3   Genomic coordinates (GRCh38) : 3:57,227,729-57,273,471 (from NCBI)


Gene-Phenotype Relationships
Location Phenotype Phenotype
MIM number
Inheritance Phenotype
mapping key
3p14.3 {Maturity-onset diabetes of the young, type 14} 616511 AD 3

TEXT

Cloning and Expression

AKT2 (164731) is a serine/threonine kinase implicated in human ovarian and pancreatic cancers. AKT2 is activated by a variety of growth factors and insulin via phosphatidylinositol 3-kinase (PIK3; see 171834). To gain insight into the function of AKT2, Mitsuuchi et al. (1999) performed yeast 2-hybrid system analysis to screen for interacting proteins. Using this technique, they identified a novel interactor, designated APPL, that contains a pleckstrin homology (PH) domain, a phosphotyrosine binding (PTB) domain, and a leucine zipper, classes of motifs defined in signaling molecules as functional interaction domains with specific targets. The PH domain of APPL shows similarity to those found in GTPase-activating proteins such as oligophrenin-1 (300127), whereas its PTB domain exhibits homology with CED-6, an adaptor protein that promotes engulfment of apoptotic cells, and IB1, a transactivator of the GLUT2 gene (138160). APPL is highly expressed in skeletal muscle, heart, ovary, and pancreas, tissues in which AKT2 mRNA is abundant.

By affinity chromatography and mass spectrometry to identify RAB5 (179512) interactors, followed by screening an adult leukocyte cDNA library, Miaczynska et al. (2004) cloned APPL1. The deduced protein contains 709 amino acids and shares 54% amino acid identity with APPL2 (606231). In addition to the central PH domain and the C-terminal PTB domain, APPL1 contains an N-terminal BAR domain.


Mapping

By fluorescence in situ hybridization, Mitsuuchi et al. (1999) mapped the APPL1 gene to 3p21.1-p14.3.


Gene Function

Mitsuuchi et al. (1999) showed that APPL interacts with the inactive form of AKT2; moreover, APPL binds to the catalytic subunit of PIK3. These data suggested that APPL is an adaptor that may tether inactive AKT2 to the PI3K in the cytoplasm and thereby may expedite recruitment of AKT2 and PI3K to the cell membrane upon mitogenic stimulation.

Miaczynska et al. (2004) identified a pathway directly linking the small GTPase RAB5, a key regulator of endocytosis, to signal transduction and mitogenesis. This pathway operated via APPL1 and APPL2, 2 RAB5 effectors that reside on a subpopulation of endosomes. In response to extracellular stimuli such as EGF (131530) and oxidative stress, APPL1 translocated from the membranes to the nucleus, where it interacted with the nucleosome remodeling and histone deacetylase (NURD) multiprotein complex, a regulator of chromatin structure and gene expression. Both APPL1 and APPL2 were essential for cell proliferation, and their function required RAB5 binding. These findings identified an endosomal compartment bearing RAB5 and APPL proteins as an intermediate in signaling between the plasma membrane and the nucleus.

Schenck et al. (2008) showed that Appl1 was widely expressed in developing zebrafish embryo with enrichment in forebrain, pronephros, and neural tube. Upon growth factor stimulation, Appl1 colocalized with Akt, and Gsk-3-beta (GSK3B; 605004) on noncanonical early endosomes beneath the plasma membrane. Knockdown of Appl1 caused apoptosis, and overexpression of Appl1 caused developmental delay and induced dysmorphic phenotypes. Overexpression of Akt2 phenocopied Appl1 overexpression. Schenck et al. (2008) showed that endosomal localization was essential for Appl1-mediated Akt activation and cell survival, and that Appl1 regulated a branch of Akt signaling in zebrafish that involves Gsk3b.


Molecular Genetics

In 2 unrelated families with maturity-onset diabetes of the young (MODY14; 616511), Prudente et al. (2015) identified heterozygosity for a nonsense mutation (L552X; 604299.0001) and a missense mutation (D94N; 604299.0002) in the APPL1 gene, respectively. Functional analysis indicated that both are loss-of-function mutations.


ALLELIC VARIANTS ( 2 Selected Examples):

.0001 MATURITY-ONSET DIABETES OF THE YOUNG, TYPE 14

APPL1, LEU552TER
  
RCV000190336

In a 4-generation Italian family with maturity-onset diabetes of the young (MODY14; 616511), Prudente et al. (2015) identified heterozygosity for a c.1655T-A transversion (c.1655T-A, NM_012096.2) in the APPL1 gene, resulting in a leu552-to-ter (L552X) substitution within the phosphotyrosine-binding (PTB) domain, predicted to cause deletion of most of the PTB domain and abolish AKT (164730) binding. Analysis of transfected HepG2 cells showed almost undetectable levels of APPL1, suggesting instability and rapid degradation of the unstable protein.


.0002 MATURITY-ONSET DIABETES OF THE YOUNG, TYPE 14

APPL1, ASP94ASN
  
RCV000190337

In a 4-generation American family with maturity-onset diabetes of the young (MODY14; 616511), Prudente et al. (2015) identified heterozygosity for a c.280G-A transition (c.280G-A, NM_012096.2) in the APPL1 gene, resulting in an asp94-to-asn (D94N) substitution at a highly conserved residue within the BAR domain. Analysis of transfected HepG2 cells showed significant reduction in enhancement of insulin-stimulated AKT (164730) and GSK3B (605004) phosphorylation with the D94N mutant compared to wildtype APPL1.


REFERENCES

  1. Miaczynska, M., Christoforidis, S., Giner, A., Shevchenko, A., Uttenweiler-Joseph, S., Habermann, B., Wilm, M., Parton, R. G., Zerial, M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116: 445-456, 2004. [PubMed: 15016378, related citations] [Full Text]

  2. Mitsuuchi, Y., Johnson, S. W., Sonoda, G., Tanno, S., Golemis, E. A., Testa, J. R. Identification of a chromosome 3p14.3-21.1 gene, APPL, encoding an adaptor molecule that interacts with the oncoprotein-serine/threonine kinase AKT2. Oncogene 18: 4891-4898, 1999. [PubMed: 10490823, related citations] [Full Text]

  3. Prudente, S., Jungtrakoon, P., Marucci, A., Ludovico, O., Buranasupkajorn, P., Mazza, T., Hastings, T., Milano, T., Morini, E., Mercuri, L., Bailetti, D., Mendonca, C., and 12 others. Loss-of-function mutations in APPL1 in familial diabetes mellitus. Am. J. Hum. Genet. 97: 177-185, 2015. [PubMed: 26073777, images, related citations] [Full Text]

  4. Schenck, A., Goto-Silva, L., Collinet, C., Rhinn, M., Giner, A., Habermann, B., Brand, M., Zerial, M. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133: 486-497, 2008. [PubMed: 18455989, related citations] [Full Text]


Marla J. F. O'Neill - updated : 8/7/2015
Patricia A. Hartz - updated : 6/6/2008
Stylianos E. Antonarakis - updated : 5/3/2004
Creation Date:
Victor A. McKusick : 11/15/1999
carol : 08/10/2015
mcolton : 8/7/2015
wwang : 6/16/2008
terry : 6/6/2008
alopez : 2/21/2007
mgross : 5/3/2004
carol : 11/16/1999

* 604299

ADAPTOR PROTEIN, PHOSPHOTYROSINE INTERACTION, PH DOMAIN, AND LEUCINE ZIPPER-CONTAINING PROTEIN 1; APPL1


Alternative titles; symbols

ADAPTOR PROTEIN CONTAINING PH DOMAIN, PTB DOMAIN, AND LEUCINE ZIPPER MOTIF 1
APPL
DIP13-ALPHA
AKT2 INTERACTOR


HGNC Approved Gene Symbol: APPL1

Cytogenetic location: 3p14.3   Genomic coordinates (GRCh38) : 3:57,227,729-57,273,471 (from NCBI)


Gene-Phenotype Relationships

Location Phenotype Phenotype
MIM number
Inheritance Phenotype
mapping key
3p14.3 {Maturity-onset diabetes of the young, type 14} 616511 Autosomal dominant 3

TEXT

Cloning and Expression

AKT2 (164731) is a serine/threonine kinase implicated in human ovarian and pancreatic cancers. AKT2 is activated by a variety of growth factors and insulin via phosphatidylinositol 3-kinase (PIK3; see 171834). To gain insight into the function of AKT2, Mitsuuchi et al. (1999) performed yeast 2-hybrid system analysis to screen for interacting proteins. Using this technique, they identified a novel interactor, designated APPL, that contains a pleckstrin homology (PH) domain, a phosphotyrosine binding (PTB) domain, and a leucine zipper, classes of motifs defined in signaling molecules as functional interaction domains with specific targets. The PH domain of APPL shows similarity to those found in GTPase-activating proteins such as oligophrenin-1 (300127), whereas its PTB domain exhibits homology with CED-6, an adaptor protein that promotes engulfment of apoptotic cells, and IB1, a transactivator of the GLUT2 gene (138160). APPL is highly expressed in skeletal muscle, heart, ovary, and pancreas, tissues in which AKT2 mRNA is abundant.

By affinity chromatography and mass spectrometry to identify RAB5 (179512) interactors, followed by screening an adult leukocyte cDNA library, Miaczynska et al. (2004) cloned APPL1. The deduced protein contains 709 amino acids and shares 54% amino acid identity with APPL2 (606231). In addition to the central PH domain and the C-terminal PTB domain, APPL1 contains an N-terminal BAR domain.


Mapping

By fluorescence in situ hybridization, Mitsuuchi et al. (1999) mapped the APPL1 gene to 3p21.1-p14.3.


Gene Function

Mitsuuchi et al. (1999) showed that APPL interacts with the inactive form of AKT2; moreover, APPL binds to the catalytic subunit of PIK3. These data suggested that APPL is an adaptor that may tether inactive AKT2 to the PI3K in the cytoplasm and thereby may expedite recruitment of AKT2 and PI3K to the cell membrane upon mitogenic stimulation.

Miaczynska et al. (2004) identified a pathway directly linking the small GTPase RAB5, a key regulator of endocytosis, to signal transduction and mitogenesis. This pathway operated via APPL1 and APPL2, 2 RAB5 effectors that reside on a subpopulation of endosomes. In response to extracellular stimuli such as EGF (131530) and oxidative stress, APPL1 translocated from the membranes to the nucleus, where it interacted with the nucleosome remodeling and histone deacetylase (NURD) multiprotein complex, a regulator of chromatin structure and gene expression. Both APPL1 and APPL2 were essential for cell proliferation, and their function required RAB5 binding. These findings identified an endosomal compartment bearing RAB5 and APPL proteins as an intermediate in signaling between the plasma membrane and the nucleus.

Schenck et al. (2008) showed that Appl1 was widely expressed in developing zebrafish embryo with enrichment in forebrain, pronephros, and neural tube. Upon growth factor stimulation, Appl1 colocalized with Akt, and Gsk-3-beta (GSK3B; 605004) on noncanonical early endosomes beneath the plasma membrane. Knockdown of Appl1 caused apoptosis, and overexpression of Appl1 caused developmental delay and induced dysmorphic phenotypes. Overexpression of Akt2 phenocopied Appl1 overexpression. Schenck et al. (2008) showed that endosomal localization was essential for Appl1-mediated Akt activation and cell survival, and that Appl1 regulated a branch of Akt signaling in zebrafish that involves Gsk3b.


Molecular Genetics

In 2 unrelated families with maturity-onset diabetes of the young (MODY14; 616511), Prudente et al. (2015) identified heterozygosity for a nonsense mutation (L552X; 604299.0001) and a missense mutation (D94N; 604299.0002) in the APPL1 gene, respectively. Functional analysis indicated that both are loss-of-function mutations.


ALLELIC VARIANTS 2 Selected Examples):

.0001   MATURITY-ONSET DIABETES OF THE YOUNG, TYPE 14

APPL1, LEU552TER
SNP: rs869320673, ClinVar: RCV000190336

In a 4-generation Italian family with maturity-onset diabetes of the young (MODY14; 616511), Prudente et al. (2015) identified heterozygosity for a c.1655T-A transversion (c.1655T-A, NM_012096.2) in the APPL1 gene, resulting in a leu552-to-ter (L552X) substitution within the phosphotyrosine-binding (PTB) domain, predicted to cause deletion of most of the PTB domain and abolish AKT (164730) binding. Analysis of transfected HepG2 cells showed almost undetectable levels of APPL1, suggesting instability and rapid degradation of the unstable protein.


.0002   MATURITY-ONSET DIABETES OF THE YOUNG, TYPE 14

APPL1, ASP94ASN
SNP: rs796065047, gnomAD: rs796065047, ClinVar: RCV000190337

In a 4-generation American family with maturity-onset diabetes of the young (MODY14; 616511), Prudente et al. (2015) identified heterozygosity for a c.280G-A transition (c.280G-A, NM_012096.2) in the APPL1 gene, resulting in an asp94-to-asn (D94N) substitution at a highly conserved residue within the BAR domain. Analysis of transfected HepG2 cells showed significant reduction in enhancement of insulin-stimulated AKT (164730) and GSK3B (605004) phosphorylation with the D94N mutant compared to wildtype APPL1.


REFERENCES

  1. Miaczynska, M., Christoforidis, S., Giner, A., Shevchenko, A., Uttenweiler-Joseph, S., Habermann, B., Wilm, M., Parton, R. G., Zerial, M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116: 445-456, 2004. [PubMed: 15016378] [Full Text: https://doi.org/10.1016/s0092-8674(04)00117-5]

  2. Mitsuuchi, Y., Johnson, S. W., Sonoda, G., Tanno, S., Golemis, E. A., Testa, J. R. Identification of a chromosome 3p14.3-21.1 gene, APPL, encoding an adaptor molecule that interacts with the oncoprotein-serine/threonine kinase AKT2. Oncogene 18: 4891-4898, 1999. [PubMed: 10490823] [Full Text: https://doi.org/10.1038/sj.onc.1203080]

  3. Prudente, S., Jungtrakoon, P., Marucci, A., Ludovico, O., Buranasupkajorn, P., Mazza, T., Hastings, T., Milano, T., Morini, E., Mercuri, L., Bailetti, D., Mendonca, C., and 12 others. Loss-of-function mutations in APPL1 in familial diabetes mellitus. Am. J. Hum. Genet. 97: 177-185, 2015. [PubMed: 26073777] [Full Text: https://doi.org/10.1016/j.ajhg.2015.05.011]

  4. Schenck, A., Goto-Silva, L., Collinet, C., Rhinn, M., Giner, A., Habermann, B., Brand, M., Zerial, M. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133: 486-497, 2008. [PubMed: 18455989] [Full Text: https://doi.org/10.1016/j.cell.2008.02.044]


Contributors:
Marla J. F. O'Neill - updated : 8/7/2015
Patricia A. Hartz - updated : 6/6/2008
Stylianos E. Antonarakis - updated : 5/3/2004

Creation Date:
Victor A. McKusick : 11/15/1999

Edit History:
carol : 08/10/2015
mcolton : 8/7/2015
wwang : 6/16/2008
terry : 6/6/2008
alopez : 2/21/2007
mgross : 5/3/2004
carol : 11/16/1999