AP1S1 defect causing MEDNIK syndrome: A new adaptinopathy associated with defective copper metabolism

Annals of the New York Academy of Sciences

Volumn 1314, Issue 1, 2014, Pages 55-63

  Martinelli, Diego ^a,b   Dionisi Vici, Carlo ^a  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Adaptinopathies; Adaptor protein complexes; AP1S1; MEDNIK syndrome

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; COPPER; MENKES PROTEIN; WILSON DISEASE PROTEIN; ZINC ACETATE;

ADAPTINOPATHY; AP1S1 GENE; ARTICLE; CELL MEMBRANE TRANSPORT; CELL ORGANELLE; COPPER METABOLISM; ENTEROPATHY; GENE; GENE MUTATION; GOLGI COMPLEX; HEARING IMPAIRMENT; HUMAN; ICHTHYOSIS; KERATODERMA; MEDNIK SYNDROME; MELANOSOME; MENKES SYNDROME; MENTAL DEFICIENCY; MENTAL RETARDATION MALFORMATION SYNDROME; NEUROPATHY; PHAKOMATOSIS; PROTEIN TRANSPORT; SKIN PIGMENTATION; SYNDROME; SYNDROME DELINEATION; WILSON DISEASE;

ADAPTINOPATHIES; ADAPTOR PROTEIN COMPLEXES; AP1S1; MEDNIK SYNDROME;

ADAPTATION, BIOLOGICAL; ADAPTOR PROTEIN COMPLEX 1; ADAPTOR PROTEIN COMPLEX SIGMA SUBUNITS; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADENOSINE TRIPHOSPHATASES; CATION TRANSPORT PROTEINS; COPPER; HEPATOLENTICULAR DEGENERATION; HUMANS; MENKES KINKY HAIR SYNDROME; PROTEIN TRANSPORT; SYNDROME; ZINC ACETATE;

EID: 84900035897     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12426     Document Type: Article

References (63)

1. de Bie, P. et al. 2007. Molecular pathogenesis of Wilson and Menkes disease: correlation of mutations with molecular defects and disease phenotypes. J. Med. Genet. 44: 673-688.
2. Kaler, S.G. 2013. Inborn errors of copper metabolism. Handb. Clin. Neurol. 113: 1745-1754.
3. Huppke, P. et al. 2012. Mutations in SLC33A1 cause a lethal autosomal-recessive disorder with congenital cataracts, hearing loss, and low serum copper and ceruloplasmin. Am. J. Hum. Genet. 90: 61-68.
4. Huppke, P. et al. 2012. Molecular and biochemical characterization of a unique mutation in CCS, the human copper chaperone to superoxide dismutase. Hum. Mutat. 33: 1207-1215.
5. Martinelli, D. et al. 2013. MEDNIK syndrome: a novel defect of copper metabolism treatable by zinc acetate therapy. Brain 136: 872-881.
6. Saba, T.G. et al. 2005. An atypical form of Erythrokeratodermia variabilis maps to chromosome 7q22. Hum. Genet. 116: 167-171.
7. Montpetit, A. et al. 2008. Disruption of AP1S1, causing a novel neurocutaneous syndrome, perturbs development of the skin and spinal cord. PLoS Genet. 4: e1000296.
8. Beare, J.M. et al. 1972. Atypical erythrokeratoderma with deafness, physical retardation and peripheral neuropathy. Br. J. Dermatol. 187: 308-314.
9. Lutsenko, S. et al. 2007. Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87: 1011-1046.
10. Jo, W.J. et al. 2008. Identification of genes involved in the toxic response of Saccharomyces cerevisiae against iron and copper overload by parallel analysis of deletion mutants. Toxicol. Sci. 101: 140-151.
11. Hung, I.H. et al. 1997. Biochemical characterization of the Wilson disease protein and functional expression in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 272: 21461-21466.
12. Petris, M.J. & J.F. Mercer . 1999. The Menkes protein (ATP7A; MNK) cycles via the plasma membrane both in basal and elevated extracellular copper using a C-terminal dileucine endocytic signal. Hum. Mol. Genet. 8: 2107-2115.
13. Lane, C. et al. 2004. Studies on endocytic mechanisms of the Menkes copper-translocating P-type ATPase (ATP7A; MNK). Endocytosis of the Menkes protein. Biometals 17: 87-98.
14. Polishchuk, R. & S. Lutsenko . 2013. Golgi in copper homeostasis: a view from the membrane trafficking field. Histochem. Cell Biol. 140: 285-295.
15. Janvier, K. et al. 2003. Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 gamma-sigma1 and AP-3 delta-sigma3 hemicomplexes. J. Cell Biol. 163: 1281-1290.
16. Coleman, S.H. et al. 2005. Leucine-specific, functional interactions between human immunodeficiency virus type 1 Nef and adaptor protein complexes. J. Virol. 79: 2066-2078.
17. Holloway, Z.G et al. 2013. Trafficking of the Menkes copper transporter ATP7A is regulated by clathrin-, AP-2-, AP-1-, and Rab22-dependent steps. Mol. Biol. Cell 24: 1735-1748.
18. Steinberg, F. et al. 2013. A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat. Cell Biol. 15: 461-471.
19. Bonifacino, J.S. & B.S. Glick . 2004. The mechanisms of vesicle budding and fusion. Cell 116: 153-166.
20. Robinson, M.S. 2004. Adaptable adaptors for coated vesicles. Trends Cell Biol. 14: 167-174.
21. Owen, D.J., B.M. Collins & P.R. Evans . 2004. Adaptors for clathrin coats: structure and function. Annu. Rev. Cell Dev. Biol. 20: 153-191.
22. Boehm, M. & J.S. Bonifacino . 2001. Adaptins: the final recount. Mol. Biol. Cell 12: 2907-2920.
23. Robinson, M.S. & J.S. Bonifacino . 2001. Adaptor-related proteins. Curr. Opin. Cell Biol. 13: 444-453.
24. Ohno, H. 2006. Clathrin-associated adaptor protein complexes. J. Cell Sci. 119: 3719-3721.
25. Robinson, M.S., D.A. Sahlender & S.D. Foster . 2010. Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev. Cell 18: 324-331.
26. Jackson, L.P. et al. 2010. A large scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141: 1220-1229.
27. Burgos, P.V. et al. 2010. Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev. Cell 18: 425 436.
28. Hirst, J. 2011. The fifth adaptor protein complex. PLoS Biol. 9: e1001170.
29. Huizing, M., R.E. Boissy & W.A. Gahl . 2002. Hermansky-Pudlak syndrome: vesicle formation from yeast to man. Pigment Cell Res. 15: 405-419.
30. Fried, K. 1972. X-linked mental retardation and/or hydrocephalus. Clin. Genet. 3: 258-263.
31. Fried, K. & R. Sanger . 1973. Possible linkage between Xg and the locus for a gene causing mental retardation with or without hydrocephalus. J. Med. Genet. 10: 17-18.
32. Carpenter, N.J. et al. 1999. Regional localization of a nonspecific X-linked mental retardation gene (MRX59) to Xp21.2-p22.2. Am. J. Med. Genet. 85: 266-270.
33. Turner, G. et al. 2003. Syndromic form of X-linked mental retardation with marked hypotonia in early life, severe mental handicap, and difficult adult behavior maps to Xp22. Am. J. Med. Genet. 117A: 245-250.
34. Tarpey, P.S. et al. 2006. Mutations in the gene encoding the sigma 2 subunit of the adaptor protein 1 complex, AP1S2, cause X-linked mental retardation. Am. J. Hum. Genet. 79: 1119-1124.
35. Saillour, Y. et al. 2007. Mutations in the AP1S2 gene encoding the sigma 2 subunit of the adaptor protein 1 complex are associated with syndromic X-linked mental retardation with hydrocephalus and calcifications in basal ganglia. J. Med. Genet. 44: 739-744.
36. McMurtry, C.T. et al. 1992. Significant developmental elevation in serum parathyroid hormone levels in a large kindred with familial benign (hypocalciuric) hypercalcemia. Am. J. Med. 93: 247-258.
37. Nesbit, M.A. et al. 2010. Identification of a second kindred with familial hypocalciuric hypercalcemia type 3 (FHH3) narrows localization to a less than 3.5 megabase pair region on chromosome 19q13.3. J. Clin. Endocrin. Metab. 95: 1947-1954.
38. Nesbit, M.A. et al. 2013. Mutations in AP2S1 cause familial hypocalciuric hypercalcemia type 3. Nat. Genet. 45: 93-97.
39. Abou Jamra, R. et al. 2011. Adaptor protein complex 4 deficiency causes severe autosomal-recessive intellectual disability, progressive spastic paraplegia, shy character, and short stature. Am. J. Hum. Genet. 88: 788-795.
40. Blumkin, L. et al. 2011. A new locus (SPG47) maps to 1p13.2-1p12 in an Arabic family with complicated autosomal recessive hereditary spastic paraplegia and thin corpus callosum. J. Neurol. Sci. 305: 67-70.
41. Moreno-De-Luca, A. et al. 2011. Adaptor protein complex-4 (AP-4) deficiency causes a novel autosomal recessive cerebral palsy syndrome with microcephaly and intellectual disability. J. Med. Genet. 48: 141-144.
42. Verkerk, A.J.M.H. et al. 2009. Mutation in the AP4M1 gene provides a model for neuroaxonal injury in cerebral palsy. Am. J. Hum. Genet. 85: 40-52.
43. Najmabadi, H. et al. 2011. Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature 478: 57-63.
44. Slabicki, M. et al. 2010. A genome-scale DNA repair RNAi screen identifies SPG48 as a novel gene associated with hereditary spastic paraplegia. PLoS Biol. 8: e1000408.
45. Giehl, K.A. et al. 2012. Nonsense mutations in AAGAB cause punctate palmoplantar keratoderma type Buschke-Fischer-Brauer. Am. J. Hum. Genet. 91:754-759.
46. Pohler, E. et al. 2012. Haploinsufficiency for AAGAB causes clinically heterogeneous forms of punctate palmoplantar keratoderma. Nat. Genet. 44:1272-1276.
47. Page, L.J. et al. 1999. Gamma-synergin: an EH domain-containing protein that interacts with gamma-adaptin. J. Cell Biol. 146: 993-1004.
48. Bonanomi, D., F. Benfenati & F. Valtorta . 2006. Protein sorting in the synaptic vesicle life cycle. Prog. Neurobiol. 80: 177-217.
49. Horikawa, H.P. et al. 2002. Interaction of synaptophysin with the AP-1 adaptor protein gamma-adaptin. Mol. Cell. Neurosci. 21: 454-462.
50. Kim, M.H. & L.B. Hersh . 2004. The vesicular acetylcholine transporter interacts with clathrin-associated adaptor complexes AP-1 and AP-2. J. Biol. Chem. 279: 12580-12587.
51. Nakagawa, T. et al.2000. A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex. Cell 103: 569-581.
52. Hirokawa, N. & R. Takemura . 2005. Molecular motors and mechanisms of directional transport in neurons. Nat. Rev. Neurosci. 6: 201-214.
53. Nakatsu, F. & H. Ohno . 2003. Adaptor protein complexes as the key regulators of protein sorting in the post-Golgi network. Cell Struct. Funct. 28: 419-429.
54. Lee, S.H. et al. 2002. Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36: 661-674.
55. Kastning, K. et al. 2007. Molecular determinants for the interaction between AMPA receptors and the clathrin adaptor complex AP-2. Proc. Natl. Acad. Sci. U. S. A. 104: 2991-2996.
56. Nakatsu F. et al. 2004. Defective function of GABA-containing synaptic vesicles in mice lacking the AP-3B clathrin adaptor. J. Cell Biol. 167: 293-302.
57. Kantheti, P. et al. 1998. Mutation in AP-3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21: 111-122.
58. Scheuber, A. et al. 2006. Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. U. S. A. 103: 16562-16567.
59. Yap, C.C. et al. 2003. Adaptor protein complex-4 (AP-4) is expressed in the central nervous system neurons and interacts with glutamate receptor delta2. Mol. Cell Neurosci. 24: 283-295.
60. Khundadze, M. et al. 2013. A hereditary spastic paraplegia mouse model supports a role of ZFYVE26/SPASTIZIN for the endolysosomal system. PLoS Genet. 9: e1003988.
61. Theos, A.C. et al. 2005. Functions of adaptor protein (AP)-3 and AP-1 in tyrosinase sorting from endosomes to melanosomes. Mol. Biol. Cell. 16: 5356-5372.
62. Chapuy, B. et al. 2008. AP-1 and AP-3 mediate sorting of melanosomal and lysosomal membrane proteins into distinct post-Golgi trafficking pathways. Traffic 9: 1157-117272.
63. Sitaram, A. et al. 2012. Differential recognition of a dileucine-based sorting signal by AP-1 and AP-3 reveals a requirement for both BLOC-1 and AP-3 in delivery of OCA2 to melanosomes. Mol. Biol. Cell. 23: 3178-3192.