Platelets of mice heterozygous for neurobeachin, a candidate gene for autism spectrum disorder, display protein changes related to aberrant protein kinase A activity

Molecular Autism

Volumn 4, Issue 1, 2013, Pages

  Nuytens, Kim ^a   Tuand, Krizia ^a   Di Michele, Michela ^b   Boonen, Kurt ^a   Waelkens, Etienne ^c   Freson, Kathleen ^a,b   Creemers, John Wm ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

Author keywords

AKAP; Autism spectrum disorder; Calpain; Candidate gene; Neurobeachin; Platelets; Serotonin; Talin 1

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALPAIN 2; COLLAGEN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; SCAFFOLD PROTEIN; TALIN; TALIN 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AUTISM; BLOOD VESSEL INJURY; CELL STRUCTURE; CONTROLLED STUDY; GENE; GENE ACTIVITY; GENE FUNCTION; GENE IDENTIFICATION; GOLGI COMPLEX; HAPLOINSUFFICIENCY; HETEROZYGOTE; MOUSE; NEUROBEACHIN GENE; NONHUMAN; PEPTIDOMICS; PHOSPHORYLATION; PKA; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SECRETORY GRANULE; THROMBOCYTE; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOCYTE RELEASE REACTION; THROMBOCYTE SHAPE; THROMBOCYTOPOIESIS;

MUS;

EID: 84886738590     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/2040-2392-4-43     Document Type: Article

References (63)

1. Etiological heterogeneity in autism spectrum disorders: more than 100 genetic and genomic disorders and still counting. Betancur C, Brain Res 2011 1380 42 77 21129364
2. Advances in autism genetics: on the threshold of a new neurobiology. Abrahams B, Geschwind D, Nat Rev Genet 2008 9 341 355 10.1038/nrg2346 18414403 (Pubitemid 351556064)
3. The neurobeachin gene is disrupted by a translocation in a patient with idiopathic autism. Castermans D, Wilquet V, Parthoens E, Huysmans C, Steyaert J, Swinnen L, Fryns JP, Van de Ven W, Devriendt K, J Med Genet 2003 40 352 356 10.1136/jmg.40.5.352 12746398 (Pubitemid 36613473)
4. Cytogenetic abnormalities and fragile-X syndrome in autism spectrum disorder. Reddy K, BMC Med Genet 2005 6 3 15655077
5. Association of autism, retinoblastoma, and reduced esterase D activity. Ritvo E, Mason-Brothers A, Menkes J, Sparkes R, Arch Gen Psychiatry 1988 45 600 10.1001/archpsyc.1988.01800300098019 3377648
6. Molecular genetic delineation of a deletion of chromosome 13q12- > q13 in a patient with autism and auditory processing deficits. Smith M, Woodroffe A, Smith R, Holguin S, Martinez J, Filipek P, Modahl C, Moore B, Bocian M, Mays L, Laulhere T, Flodman P, Spence MA, Cytogenet Genome Res 2002 98 233 239 10.1159/000071040 12826745 (Pubitemid 37499851)
7. An evidence-based approach to establish the functional and clinical significance of copy number variants in intellectual and developmental disabilities. Kaminsky EB, Kaul V, Paschall J, Church DM, Bunke B, Kunig D, Moreno-De-Luca D, Moreno-De-Luca A, Mulle JG, Warren ST, Richard G, Compton JG, Fuller AE, Gliem TJ, Huang S, Collinson MN, Beal SJ, Ackley T, Pickering DL, Golden DM, Aston E, Whitby H, Shetty S, Rossi MR, Rudd MK, South ST, Brothman AR, Sanger WG, Iyer RK, Crolla JA, et al. Genet Med 2011 13 777 784 10.1097/GIM.0b013e31822c79f9 21844811
8. Use of array CGH to detect exonic copy number variants throughout the genome in autism families detects a novel deletion in TMLHE. Celestino-Soper PB, Shaw CA, Sanders SJ, Li J, Murtha MT, Ercan-Sencicek AG, Davis L, Thomson S, Gambin T, Chinault AC, Ou Z, German JR, Milosavljevic A, Sutcliffe JS, Cook EH Jr, Stankiewicz P, State MW, Beaudet AL, Hum Mol Genet 2011 20 4360 4370 10.1093/hmg/ddr363 21865298
9. Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism. Sanders SJ, Ercan-Sencicek AG, Hus V, Luo R, Murtha MT, Moreno-De-Luca D, Chu SH, Moreau MP, Gupta AR, Thomson SA, Mason CE, Bilguvar K, Celestino-Soper PB, Choi M, Crawford EL, Davis L, Wright NR, Dhodapkar RM, DiCola M, DiLullo NM, Fernandez TV, Fielding-Singh V, Fishman DO, Frahm S, Garagaloyan R, Goh GS, Kammela S, Klei L, Lowe JK, Lund SC, et al. Neuron 2011 70 863 885 10.1016/j.neuron.2011. 05.002 21658581
10. A discovery resource of rare copy number variations in individuals with autism spectrum disorder. Prasad A, Merico D, Thiruvahindrapuram B, Wei J, Lionel AC, Sato D, Rickaby J, Lu C, Szatmari P, Roberts W, Fernandez BA, Marshall CR, Hatchwell E, Eis PS, Schrerer SW, G3 (Bethesda) 2012 2 1665 1685 2012 23275889
11. A genome-wide scan for common alleles affecting risk for autism. Anney R, Klei L, Pinto D, Regan R, Conroy J, Magalhaes TR, Correia C, Abrahams BS, Sykes N, Pagnamenta AT, Almeida J, Baccheli E, Bailey AJ, Baird G, Battaglia A, Berney T, Bolshakova N, Bölte S, Bolton PF, Bourgeron T, Brennan S, Brian J, Carson AR, Casallo G, Casey J, Chu SH, Cochrane L, Corsello C, Crawford EL, Crossett A, et al. Hum Mol Genet 2010 19 4072 4082 10.1093/hmg/ddq307 20663923
12. An autosomal genomic screen for autism. Collaborative linkage study of autism. Barrett S, Beck J, Bernier R, Bisson E, Braun T, Casavant T, Childress D, Folstein S, Garcia M, Gardiner M, Gilman S, Haines JL, Hopkins K, Landa R, Meyer NH, Mullane JA, Nishimura DY, Palmer P, Piven J, Purdy J, Santangelo SL, Searby C, Sheffield V, Singleton J, Slager S, Struchen T, Svenson S, Vieland V, Wang K, Winklosky B, Am J Med Genet 1999 88 609 615 10581478
13. Incorporating language phenotypes strengthens evidence of linkage to autism. Bradford Y, Haines J, Hutcheson H, Gardiner M, Braun T, Sheffield V, Cassavant T, Huang W, Wang K, Vieland V, Folstein S, Santangelo S, Piven J, Am J Med Genet 2001 105 539 547 10.1002/ajmg.1497 (Pubitemid 32729823)
14. The neurobeachin gene spans the common fragile site FRA13A. Savelyeva L, Sagulenko E, Schmitt J, Schwab M, Hum Genet 2006 118 551 558 10.1007/s00439-005-0083-z 16244873 (Pubitemid 41825127)
15. The autism candidate gene neurobeachin encodes a scaffolding protein implicated in membrane trafficking and signaling. Volders K, Nuytens K, Creemers JW, Curr Mol Med 2011 11 204 217 10.2174/156652411795243432 21375492
16. Neurobeachin: a protein kinase A-anchoring, beige/chediak-higashi protein homolog implicated in neuronal membrane traffic. Wang X, Herberg FW, Laue MM, Wullner C, Hu B, Petrasch-Parwez E, Kilimann MW, J Neurosci 2000 20 8551 8565
17. New insights into clostridial neurotoxin-SNARE interactions. Breidenbach M, Brunger A, Trends Mol Med 2005 11 377 381 10.1016/j.molmed.2005.06.012 16006188 (Pubitemid 41080579)
18. A concanavalin A-like lectin domain in the CHS1/LYST protein, shared by members of the BEACH family. Burgess A, Mornon JP, de Saint-Basile G, Callebaut I, Bioinformatics 2009 25 1219 1222 10.1093/bioinformatics/btp151 19289442
19. Crystal structure of the PH-BEACH domains of human LRBA/BGL. Gebauer D, Li J, Jogl G, Shen Y, Myszka D, Tong L, Biochemistry 2004 43 14873 14880 10.1021/bi049498y 15554694 (Pubitemid 39587463)
20. BEACH family of proteins: phylogenetic and functional analysis of six dictyostelium BEACH proteins. Wang N, Wu WI, De Lozanne A, J Cell Biochem 2002 86 561 570 10.1002/jcb.10254 12210762 (Pubitemid 36076172)
21. Neurobeachin is essential for neuromuscular synaptic transmission. Su Y, Balice-Gordon RJ, Hess DM, Landsman DS, Minarcik J, Golden J, Hurwitz I, Liebhaber SA, Cooke NE, J Neurosci 2004 24 3627 3636 10.1523/JNEUROSCI.4644-03. 2004 15071111 (Pubitemid 38481120)
22. Dendritic spine formation and synaptic function require neurobeachin. Niesmann K, Breuer D, Brockhaus J, Born G, Wolff I, Reissner C, Kilimann MW, Rohlmann A, Missler M, Nat Commun 2011 2 557 22109531
23. Neurobeachin regulates neurotransmitter receptor trafficking to synapses. Nair R, Lauks J, Jung S, Cooke NE, de Wit H, Brose N, Kilimann MW, Verhage M, Rhee J, J Cell Biol 2013 200 61 80 10.1083/jcb.201207113 23277425
24. SCAMP5, NBEA and AMISYN: three candidate genes for autism involved in secretion of large dense-core vesicles. Castermans D, Volders K, Crepel A, Backx L, De Vos R, Freson K, Meulemans S, Vermeesch JR, Schrander-Stumpel CT, De Rijk P, Del-Favero J, Van Geet C, Hum Mol Genet 2010 19 1368 1378 10.1093/hmg/ddq013 20071347
25. Molecular mechanisms of platelet exocytosis: insights into the "secrete" life of thrombocytes. Reed GL, Fitzgerald ML, Polgar J, Blood 2000 96 3334 3342 11071625
26. Regulated granule trafficking in platelets and neurons: a common molecular machinery. Goubau C, Buyse GM, Di Michele M, Van Geet C, Freson K, Eur J Paediatr Neurol 2012 17 2 117 125 22951324
27. Blood platelets as neuronal models: use and limitations. Pletscher A, Clin Neuropharmacol 1986 9 Suppl 4 344 346 3032430
28. Exome sequencing identifies NBEAL2 as the causative gene for gray platelet syndrome. Albers CA, Cvejic A, Favier R, Bouwmans EE, Alessi MC, Bertone P, Jordan G, Kettleborough RN, Kiddle G, Kostadima M, Read RJ, Sipos B, Sivapalaratnam S, Smethurst PA, Stephens J, Voss K, Nurden A, Rendon A, Nurden P, Ouwehand WH, Nat Genet 2011 43 735 737 10.1038/ng.885 21765411
29. Clinical, molecular, and cell biological aspects of chediak-higashi syndrome. Introne W, Boissy RE, Gahl WA, Mol Genet Metab 1999 68 283 303 10.1006/mgme.1999.2927 10527680 (Pubitemid 29501101)
30. Hyperserotonemia in autism: activity of 5HT-associated platelet proteins. Hranilovic D, Bujas-Petkovic Z, Tomicic M, Bordukalo-Niksic T, Blazevic S, Cicin-Sain L, J Neural Transm 2009 116 493 501 10.1007/s00702-009-0192-2 19221690
31. An integrated proteomics and genomics analysis to unravel a heterogeneous platelet secretion defect. Di Michele M, Thys C, Waelkens E, Overbergh L, D'Hertog W, Mathieu C, De Vos R, Peerlinck K, Van Geet C, Freson K, J Proteomics 2011 74 902 913 10.1016/j.jprot.2011.03.007 21406263
32. The pituitary adenylate cyclase-activating polypeptide is a physiological inhibitor of platelet activation. Freson K, Hashimoto H, Thys C, Wittevrongel C, Danloy S, Morita Y, Shintani N, Tomiyama Y, Vermylen J, Hoylaerts MF, Baba A, Van Geet C, J Clin Invest 2004 113 905 912 15067323 (Pubitemid 38544149)
33. The TUBB1 Q43P functional polymorphism reduces the risk of cardiovascular disease in men by modulating platelet function and structure. Freson K, De Vos R, Wittevrongel C, Thys C, Defoor J, Vanhees L, Vermylen J, Peerlinck K, Van Geet C, Blood 2005 106 2356 2362 10.1182/blood-2005-02-0723 15956286 (Pubitemid 41510807)
34. Platelet ultrastructural morphometry for diagnosis of partial delta-storage pool disease in patients with mild platelet dysfunction and/or thrombocytopenia of unknown origin. A study of 24 cases. Pujol-Moix N, Hernandez A, Escolar G, Espanol I, Martinez-Brotons F, Mateo J, Haematologica 2000 85 619 626 10870119 (Pubitemid 30450942)
35. Heterogeneous abnormalities of platelet dense granule ultrastructure in 20 patients with congenital storage pool deficiency. Weiss HJ, Lages B, Vicic W, Tsung LY, White JG, Br J Haematol 1993 83 282 295 10.1111/j.1365-2141.1993. tb08284.x 8457477 (Pubitemid 23060926)
36. Identification and relative quantification of neuropeptides from the endocrine tissues. Boonen K, Husson SJ, Landuyt B, Baggerman G, Hayakawa E, Luyten WH, Schoofs L, Methods Mol Biol 2010 615 191 206 10.1007/978-1-60761-535- 4-15 20013210
37. Molecular mechanisms of SERT in platelets: regulation of plasma serotonin levels. Mercado CP, Kilic F, Mol Interv 2010 10 231 241 10.1124/mi.10.4.6 20729489
38. Platelet signaling. Stalker TJ, Newman DK, Ma P, Wannemacher KM, Brass LF, Handb Exp Pharmacol 2012 210 59 85 10.1007/978-3-642-29423-5-3 22918727
39. Neurobeachin, a protein implicated in membrane protein traffic and autism, is required for the formation and functioning of central synapses. Medrihan L, Rohlmann A, Fairless R, Andrae J, Doring M, Missler M, Zhang W, Kilimann MW, J Physiol 2009 587 5095 5106 10.1113/jphysiol.2009.178236 19723784
40. Haploinsufficiency of the autism candidate gene neurobeachin induces autism-like behaviors and affects cellular and molecular processes of synaptic plasticity in mice. Nuytens K, Gantois I, Stijnen P, Iscru E, Laeremans A, Serneels L, Van Eylen L, Liebhaber SA, Devriendt K, Balschun D, Arckens L, Creemers JW, D'Hooge R, Neurobiol Dis 2013 51 144 151 23153818
41. Peptidomic analysis of human blood specimens: comparison between plasma specimens and serum by differential peptide display. Tammen H, Schulte I, Hess R, Menzel C, Kellmann M, Mohring T, Schulz-Knappe P, Proteomics 2005 5 3414 3422 10.1002/pmic.200401219 16038021 (Pubitemid 41192047)
42. Spectral clustering in peptidomics studies helps to unravel modification profile of biologically active peptides and enhances peptide identification rate. Menschaert G, Vandekerckhove TT, Landuyt B, Hayakawa E, Schoofs L, Luyten W, Van Criekinge W, Proteomics 2009 9 4381 4388 10.1002/pmic.200900248 19658089
43. Talin contains a C-terminal calpain2 cleavage site important in focal adhesion dynamics. Bate N, Gingras AR, Bachir A, Horwitz R, Ye F, Patel B, Goult BT, Critchley DR, PLoS One 2012 7 34461 10.1371/journal.pone.0034461 22496808
44. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Franco SJ, Rodgers MA, Perrin BJ, Han J, Bennin DA, Critchley DR, Huttenlocher A, Nat Cell Biol 2004 6 977 983 10.1038/ncb1175 15448700 (Pubitemid 39359850)
45. Calpains: an elaborate proteolytic system. Ono Y, Sorimachi H, Biochim Biophys Acta 2012 1824 224 236 10.1016/j.bbapap.2011.08.005 21864727
46. Activation of m-calpain (calpain II) by epidermal growth factor is limited by protein kinase A phosphorylation of m-calpain. Shiraha H, Glading A, Chou J, Jia Z, Wells A, Mol Cell Biol 2002 22 2716 2727 10.1128/MCB.22.8.2716- 2727.2002 11909964 (Pubitemid 34262992)
47. Glutamate substitutions at a PKA consensus site are consistent with inactivation of calpain by phosphorylation. Smith SD, Jia Z, Huynh KK, Wells A, Elce JS, FEBS Lett 2003 542 115 118 10.1016/S0014-5793(03)00361-2 12729909 (Pubitemid 36555725)
48. The effects of disruption of a kinase anchoring protein-protein kinase A association on protein kinase A signalling in neuroendocrine melanotroph cells of Xenopus laevis. Corstens GJ, van Boxtel R, van den Hurk MJ, Roubos EW, Jenks BG, J Neuroendocrinol 2006 18 477 483 10.1111/j.1365-2826.2006.01439.x 16774496 (Pubitemid 43821719)
49. Serotonergic disturbances in autistic disorder: L-5-hydroxytryptophan administration to autistic youngsters increases the blood concentrations of serotonin in patients but not in controls. Croonenberghs J, Verkerk R, Scharpe S, Deboutte D, Maes M, Life Sci 2005 76 2171 2183 10.1016/j.lfs.2004.06.032 15733932 (Pubitemid 40283642)
50. Statistical distribution of blood serotonin as a predictor of early autistic brain abnormalities. Janusonis S, Theor Biol Med Model 2005 2 27 10.1186/1742-4682-2-27 16029508 (Pubitemid 41259093)
51. Platelet serotonin studies in hyperserotonemic relatives of children with autistic disorder. Cook EH Jr, Arora RC, Anderson GM, Berry-Kravis EM, Yan SY, Yeoh HC, Sklena PJ, Charak DA, Leventhal BL, Life Sci 1993 52 2005 2015 10.1016/0024-3205(93)90685-V 7684805
52. Increased Gs signalling in platelets and impaired collagen activation, due to a defect in the dystrophin gene, result in increased blood loss during spinal surgery. Labarque V, Freson K, Thys C, Wittevrongel C, Hoylaerts MF, De Vos R, Goemans N, Van Geet C, Hum Mol Genet 2008 17 357 366 17981813
53. SM22beta Encodes a lineage-restricted cytoskeletal protein with a unique developmentally regulated pattern of expression. Zhang JC, Helmke BP, Shum A, Du K, Yu WW, Lu MM, Davies PF, Parmacek MS, Mech Dev 2002 115 161 166 10.1016/S0925-4773(02)00088-6 12049783 (Pubitemid 34615683)
54. Thymosin beta 10 and thymosin beta 4 are both actin monomer sequestering proteins. Yu FX, Lin SC, Morrison-Bogorad M, Atkinson MA, Yin HL, J Biol Chem 1993 268 502 509 8416954 (Pubitemid 23021350)
55. A C-terminal dimerization motif is required for focal adhesion targeting of Talin1 and the interaction of the Talin1 I/LWEQ module with F-actin. Smith SJ, McCann RO, Biochemistry 2007 46 10886 10898 10.1021/bi700637a 17722883 (Pubitemid 47463040)
56. Characterization of an actin-binding site within the talin FERM domain. Lee HS, Bellin RM, Walker DL, Patel B, Powers P, Liu H, Garcia-Alvarez B, de Pereda JM, Liddington RC, Volkmann N, Hanein D, Critchley DR, Robson RM, J Mol Biol 2004 343 771 784 10.1016/j.jmb.2004.08.069 15465061 (Pubitemid 39311621)
57. Talin binding to integrin beta tails: a final common step in integrin activation. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, de Pereda JM, Ginsberg MH, Calderwood DA, Science 2003 302 103 106 10.1126/science.1086652 14526080 (Pubitemid 37210697)
58. Loss of talin1 in platelets abrogates integrin activation, platelet aggregation, and thrombus formation in vitro and in vivo. Nieswandt B, Moser M, Pleines I, Varga-Szabo D, Monkley S, Critchley D, Fassler R, J Exp Med 2007 204 3113 3118 10.1084/jem.20071827 18086864
59. A unique talin antigenic determinant and anomalous megakaryocyte talin distribution associated with abnormal platelet formation in the wistar furth rat. Jackson CW, Hutson NK, Steward SA, Stenberg PE, Blood 1992 79 1729 1737 1373085
60. Wistar furth rat megakaryocytes lack dense compartments and intercellular plaques, membranous structures rich in cytoskeletal proteins. Stenberg PE, Beckstead JH, Jackson CW, Cell Adhes Commun 1998 5 397 407 10.3109/ 15419069809010784 9789686
61. A noise-reduction GWAS analysis implicates altered regulation of neurite outgrowth and guidance in autism. Hussman JP, Chung RH, Griswold AJ, Jaworski JM, Salyakina D, Ma D, Konidari I, Whitehead PL, Vance JM, Martin ER, Cuccaro ML, Gilbert JR, Haines JL, Pericak-Vance MA, Mol Autism 2011 2 1 10.1186/2040-2392-2-1 21247446
62. Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Gilman SR, Iossifov I, Levy D, Ronemus M, Wigler M, Vitkup D, Neuron 2011 70 898 907 10.1016/j.neuron.2011.05.021 21658583
63. AKAPs integrate genetic findings for autism spectrum disorders. Poelmans G, Franke B, Pauls DL, Glennon JC, Buitelaar JK, Transl Psychiatry 2013 3 270 10.1038/tp.2013.48 23756379