*103320
AGRIN; AGRN

HGNC Approved Gene Symbol: AGRN

Cytogenetic location: 1p36.33     Genomic coordinates (GRCh37): 1:955,502 - 991,491 (from NCBI)

Gene Phenotype Relationships
Location Phenotype Phenotype
MIM number
1p36.33 Myasthenia, limb-girdle, familial 254300

TEXT
Description
Agrin is a neuronal aggregating factor that induces the aggregation of acetylcholine receptors and other postsynaptic proteins on muscle fibers and is crucial for the formation of the neuromuscular junction.

Cloning
Rupp et al. (1991) isolated cDNAs from a rat embryonic spinal cord library using an agrin cDNA clone isolated from electromotor neurons of a marine ray. Analysis of a set of clones predicted a protein with 1,940 amino acids, including 141 cysteine residues. The predicted protein had 9 domains homologous to protease inhibitors, a region similar to domain III of laminin (see 150240), and 4 epidermal growth factor (131530) repeats. The gene was expressed in rat embryonic nervous system and muscle. The protein was concentrated at synapses. Rupp et al. (1992) described alternative RNA splicing in mammalian agrin resulting in many extracellular matrix protein isoforms.

Mapping
Rupp et al. (1992) mapped the human AGRN gene to 1pter-p32 by analysis of Chinese hamster/human somatic cell hybrids, including one that carried chromosome 1 region p32-qter (which was negative for the human signal). The mouse gene was mapped to chromosome 4 by study of Chinese hamster/mouse somatic cell hybrids. Thus, this is another example of extensive homology of synteny between 1pter-p32 and the distal half of mouse chromosome 4. Three neurologic mutants in that region of mouse chromosome 4 were pointed to as possible candidate diseases for mutations in the Agrn gene.

Gene Function
An important event in synapse formation is the accumulation of neurotransmitter receptors beneath the presynaptic nerve terminal. Agrin is a component of the synaptic basal lamina that induces the clustering (aggregation) of acetylcholine receptors (e.g., 100690) on cultured muscle fibers. Campanelli et al. (1991) showed that when a cDNA encoding a putative agrin protein is transfected into cells, the molecule is secreted and concentrated on the extracellular surface. Coculture of transfected cells with muscle fibers induced formation of receptor patches at contact sites. These results demonstrated that expression of a single gene encoding agrin confers receptor clustering that is restricted to specific sites of contact between the synthesizing cell and muscle. DeChiara et al. (1996) showed that agrin acts through the skeletal muscle tyrosine kinase receptor MuSK (601296) to activate signaling cascades responsible for all aspects of synapse formation, including organization of the postsynaptic membrane, synapse-specific transcription, and presynaptic differentiation. In mouse muscle and cultured myotube cells, Finn et al. (2003) showed that the tyrosine kinases Abl1 (189980) and Abl2 (164690) are concentrated at the postsynaptic neuromuscular junction and are mediators of postsynaptic AChR clustering downstream of agrin and MuSK signaling. The authors suggested that the Abl kinases influence cytoskeletal regulatory molecules important for synapse assembly and remodeling.

In cultured myocytes, Wang et al. (2003) found that agrin-induced AChR postsynaptic aggregation required the tumor suppressor gene APC (611731), which was found to colocalize and bind specifically to the AChR beta subunit (100710). The interaction occurred downstream of MuSK activation. Wang et al. (2003) suggested that a direct interaction between APC and the AChR beta subunit may link AChR to the cytoskeleton, helping to localize the receptors to the neuromuscular junction.

T-cell activation is dependent on both a primary signal delivered through the T-cell receptor and a secondary costimulatory signal mediated by coreceptors. Costimulation is thought to act through the specific redistribution and clustering of membrane and intracellular kinase-rich lipid raft microdomains at the contact site between T cells and antigen-presenting cells. This site has been termed the immunologic synapse. Khan et al. (2001) demonstrated that agrin, an aggregating protein crucial for formation of the neuromuscular junction, is also expressed in lymphocytes and is important in reorganization of membrane lipid microdomains and setting the threshold for T-cell signaling. Khan et al. (2001) concluded that agrin induces the aggregation of signaling proteins and the creation of signaling domains in both immune and nervous systems through a common lipid raft pathway.

In addition to its role at the neuromuscular junction, agrin has been implicated in brain development. Through biochemical studies, Hilgenberg et al. (2006) found that agrin bound the alpha-3 subunit of the Na(+)/K(+)-ATPase (ATP1A3; 182350) in mouse cortical neurons. Immunohistochemical analysis showed that Atp1a3 colocalized with agrin-binding sites at synapses. Agrin inhibited Atp1a3 activity, resulting in membrane depolarization and increased action potential frequency in mouse cortical neurons in culture and acute slice. An agrin fragment that acted as a competitive antagonist depressed action potential frequency, indicating that endogenous agrin regulates native Atp1a3 function. Hilgenberg et al. (2006) concluded that agrin regulates activity-dependent processes in neurons through its interaction with ATP1A3.

Molecular Genetics
In a Swiss brother and sister with congenital myasthenic syndrome (254300), Huze et al. (2009) identified a homozygous mutation in the AGRN gene (G1709R; 103320.0001). Mutant agrin was expressed and localized correctly in patient muscle, but the overall organization of the neuromuscular junction was perturbed, affecting both the pre- and postsynaptic regions. AChR clustering and density was not affected. The findings suggested that agrin also helps to maintain the neuromuscular junction.

Animal Model
Data on the structure, expression, and bioactivity of agrin all support the notion that it plays a central role in regulating postsynaptic differentiation. However, agrin is only one of several agents that can cause clustering of acetylcholine receptors in vitro. To test critically the 'agrin hypothesis' (McMahan, 1990), Gautam et al. (1996) generated knockout mice deficient for agrin and showed that neuromuscular differentiation is grossly defective in these mice. Some postsynaptic differentiation occurred in the mutant, suggesting the existence of a second nerve-derived synaptic organizing signal.

Formation of the neuromuscular junction depends upon reciprocal inductive interactions between the developing nerve and muscle, resulting in the precise juxtaposition of a differentiated nerve terminal with a highly specialized patch on the muscle membrane, termed the motor endplate. Agrin is a nerve-derived factor involved in induction of the molecular reorganization at the motor endplate. Glass et al. (1996) found that mice lacking either agrin or the receptor tyrosine kinase MuSK (601296) exhibit similar profound defects at the neuromuscular junction. DeChiara et al. (1996) showed in knockout mice that MuSK is required for formation of the neuromuscular junction in vivo.

Lin et al. (2001) analyzed early stages of postsynaptic differentiation in muscles of mutant mice lacking agrin, MuSK, rapsyn (601592), and/or motor nerves. Lin et al. (2001) found that the defect in MuSK mutants is due to an absence of initiation of postsynaptic differentiation, whereas the impairment in agrin mutants is caused by loss of agrin-dependent maintenance of the postsynaptic apparatus. On the basis of these and previous studies, Lin et al. (2001) proposed the existence of 3 early overlapping steps in the formation of the postsynaptic apparatus at the neuromuscular junction. First, a muscle-intrinsic, nerve/agrin-independent and MuSK-dependent mechanism initiates formation of postsynaptic specialization in an end-plate band. Second, nerve-derived agrin acts through MuSK to promote apposition of nerve terminals to these nerve-independent acetylcholine receptor clusters and/or to induce new postsynaptic sites. Agrin is also required for the growth and maintenance of most, if not all, synaptic sites. Third, motor axons, or Schwann cells that accompany them, provide an agrin-independent signal that destabilizes or disperses postsynaptic apparatus that have not been stabilized by agrin.

ALLELIC VARIANTS (Selected Examples):

.0001 MYASTHENIA, LIMB-GIRDLE, FAMILIAL
AGRN, GLY1709ARG

In a sister and brother with congenital myasthenic syndrome mostly affecting the limb-girdle muscles (254300), Huze et al. (2009) identified a homozygous 5125G-C transversion in exon 29 of the AGRN gene, resulting in a gly1709-to-arg (G1709R) substitution in the C-terminal laminin G-like 2 (LG2) domain. Both patients were unable to run since childhood and had mild muscle weakness as adults. Neither had diplopia, bulbar symptoms, or dyspnea. The mutation was not found in 200 control alleles. Skeletal muscle biopsy showed pre- and postsynaptic defects at the neuromuscular junction (NMJ), although mutant agrin staining was localized correctly. In vitro functional expression studies in myotubes showed that mutant agrin did not significantly impair AChR clustering, activation of MuSK (601296), or the interaction with alpha-dystroglycan (DAG; 128239). Injection of the mutant protein into rat muscle did not affect AChR recruit or expression at the NMJ. However, the NMJ showed remodeling and denervation: the presynaptic department had disheveled neurofilaments, and the postsynaptic compartment had increased synaptic gutter fragments. Huze et al. (2009) concluded that the mutant agrin destabilized the preexisting NMJ, suggesting that wildtype agrin is involved in the maintenance of the NMJ.

REFERENCES
1. Campanelli, J. T., Hoch, W., Rupp, F., Kreiner, T., Scheller, R. H. Agrin mediates cell contact-induced acetylcholine receptor clustering. Cell 67: 909-916, 1991. [PubMed: 1659950, related citations] [Full Text: Elsevier Science, Pubget]

2. DeChiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., Kinetz, E., Compton, D. L., Rojas, E., Park, J. S., Smith, C., DiStefano, P. S., Glass, D. J., Burden, S. J., Yancopoulos, G. D. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85: 501-512, 1996. [PubMed: 8653786, related citations] [Full Text: Elsevier Science, Pubget]

3. DeChiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., Kinetz, E., Compton, D. L., Rojas, E., Park, J. S., Smith, C., DiStefano, P. S., Glass, D. J., Burden, S. J., Yancopoulos, G. D. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85: 501-512, 1996. [PubMed: 8653786, related citations] [Full Text: Elsevier Science, Pubget]

4. Finn, A. J., Feng, G., Pendergast, A. M. Postsynaptic requirement for Abl kinases in assembly of the neuromuscular junction. Nature Neurosci. 6: 717-723, 2003. [PubMed: 12796783, related citations] [Full Text: Nature Publishing Group, Pubget]

5. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P., Sanes, J. R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85: 525-535, 1996. [PubMed: 8653788, related citations] [Full Text: Elsevier Science, Pubget]

6. Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J., DiStefano, P. S., Valenzuela, D. M., DeChiara, T. M., Yancopoulos, G. D. Agrin acts via a MuSK receptor complex. Cell 85: 513-523, 1996. [PubMed: 8653787, related citations] [Full Text: Elsevier Science, Pubget]

7. Hilgenberg, L. G. W., Su, H., Gu, H., O'Dowd, D. K., Smith, M. A. Alpha-3-Na(+)/K(+)-ATPase is a neuronal receptor for agrin. Cell 125: 359-369, 2006. [PubMed: 16630822, related citations] [Full Text: Elsevier Science, Pubget]

8. Huze, C., Bauche, S., Richard, P., Chevessier, F., Goillot, E., Gaudon, K., Ben Ammar, A., Chaboud, A., Grosjean, I., Lecuyer, H.-A., Bernard, V., Rouche, A., and 10 others. Identification of an agrin mutation that causes congenital myasthenia and affects synapse function. Am. J. Hum. Genet. 85: 155-167, 2009. Note: Erratum: Am. J. Hum. Genet. 85: 536 only, 2009. [PubMed: 19631309, related citations] [Full Text: Elsevier Science, Pubget]

9. Khan, A. A., Bose, C., Yam, L. S., Soloski, M. J., Rupp, F. Physiological regulation of the immunological synapse by agrin. Science 292: 1681-1686, 2001. [PubMed: 11349136, related citations] [Full Text: HighWire Press, Pubget]

10. Lin, W., Burgess, R. W., Dominguez, B., Pfaff, S. L., Sanes, J. R., Lee, K.-F. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410: 1057-1064, 2001. [PubMed: 11323662, related citations] [Full Text: Nature Publishing Group, Pubget]

11. McMahan, U. J. The agrin hypothesis Cold Spring Harb. Symp. Quant. Biol. 50: 407-418, 1990.

12. Rupp, F., Ozcelik, T., Linial, M., Peterson, K., Francke, U., Scheller, R. Structure and chromosomal localization of the mammalian agrin gene. J. Neurosci. 12: 3535-3544, 1992. [PubMed: 1326608, related citations] [Full Text: HighWire Press, Pubget]

13. Rupp, F., Payan, D. G., Magill-Solc, C., Cowan, D. M., Scheller, R. H. Structure and expression of a rat agrin. Neuron 6: 811-823, 1991. [PubMed: 1851019, related citations] [Full Text: Elsevier Science, Pubget]

14. Wang, J., Jing, Z., Zhang, L., Zhou, G., Braun, J., Yao, Y., Wang, Z.-Z. Regulation of acetylcholine receptor clustering by the tumor suppressor APC. Nature Neurosci. 6: 1017-1018, 2003. [PubMed: 14502292, related citations] [Full Text: Nature Publishing Group, Pubget]

Contributors: Matthew B. Gross - updated : 3/8/2010
Cassandra L. Kniffin - updated : 10/9/2009
Cassandra L. Kniffin - updated : 10/9/2003
Cassandra L. Kniffin - updated : 6/20/2003
Ada Hamosh - updated : 6/12/2001
Ada Hamosh - updated : 4/23/2001
Creation Date: Victor A. McKusick : 12/17/1991
Edit History: wwang : 03/11/2010
mgross : 3/8/2010
wwang : 10/16/2009
wwang : 10/16/2009
wwang : 10/16/2009
ckniffin : 10/9/2009
ckniffin : 2/5/2008
alopez : 7/28/2006
terry : 7/24/2006
carol : 10/13/2003
ckniffin : 10/9/2003
alopez : 7/28/2003
carol : 6/23/2003
ckniffin : 6/20/2003
alopez : 6/13/2001
terry : 6/12/2001
alopez : 4/25/2001
terry : 4/23/2001
terry : 6/6/1996
terry : 6/4/1996
carol : 3/31/1994
carol : 12/9/1993
supermim : 3/16/1992
carol : 2/17/1992
carol : 12/17/1991