ACTG2 variants impair actin polymerization in sporadic Megacystis Microcolon Intestinal Hypoperistalsis Syndrome

Human Molecular Genetics

Volumn 25, Issue 3, 2016, Pages 571-583

  Halim, Danny ^a   Hofstra, Robert M W ^a,f   Signorile, Luca ^a   Verdijk, Rob M ^a   Van Der Werf, Christine S ^b   Sribudiani, Yunia ^a,g   Brouwer, Rutger W W ^a   van IJcken, Wilfred F J ^a   Dahl, Niklas ^c   Verheij, Joke B G M ^b   Baumann, Clarisse ^d   Kerner, John ^e   Van Bever, Yolande ^a   Galjart, Niels ^a   Wijnen, Rene M H ^a   Tibboel, Dick ^a   Burns, Alan J ^a,f   Muller, Françoise ^d   Brooks, Alice S ^a   Alves, Maria M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UPPSALA UNIVERSITY   (Sweden)

^d HÔPITAL ROBERT DEBRÉ   (France)

^e STANFORD UNIVERSITY   (United States)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g PADJADJARAN UNIVERSITY   (Indonesia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTG2 PROTEIN; DNA; SMOOTH MUSCLE ACTIN; UNCLASSIFIED DRUG; ACTG2 PROTEIN, HUMAN; ACTIN;

ACTIN POLYMERIZATION; AMINO ACID SUBSTITUTION; ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; COLON DISEASE; CONGENITAL DISORDER; CONTROLLED STUDY; CRYSTAL STRUCTURE; EXON; FEMALE; FETUS; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC VARIABILITY; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTESTINE OBSTRUCTION; MALE; MEGACYSTIS MICROCOLON INTESTINAL HYPOPERISTALSIS SYNDROME; MISSENSE MUTATION; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; SMOOTH MUSCLE CONTRACTILITY; SMOOTH MUSCLE FIBER; SYNDROME; ABNORMALITIES; BLADDER; CASE REPORT; CHEMISTRY; COLON; FATALITY; GENETICS; INTESTINE; INTESTINE PSEUDOOBSTRUCTION; METABOLISM; MULTIPLE MALFORMATION SYNDROME; MUSCLE CONTRACTION; NEWBORN; PATHOLOGY; PEDIGREE; PROTEIN MULTIMERIZATION; SMOOTH MUSCLE; YOUNG ADULT;

ABNORMALITIES, MULTIPLE; ACTINS; COLON; FATAL OUTCOME; FEMALE; GENE EXPRESSION; HETEROZYGOTE; HUMANS; INFANT, NEWBORN; INTESTINAL PSEUDO-OBSTRUCTION; INTESTINES; MALE; MOLECULAR DYNAMICS SIMULATION; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MUTATION, MISSENSE; PEDIGREE; PROTEIN MULTIMERIZATION; URINARY BLADDER; YOUNG ADULT;

EID: 84960906224     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv497     Document Type: Article

References (32)

1. Berdon, W.E., Baker, D.H., Blanc, W.A., Gay, B., Santulli, T.V. and Donovan, C. (1976) Megacystis-microcolon-intestinal hypoperistalsis syndrome: a newcause of intestinal obstruction in the newborn. Report of radiologic findings in five newborn girls. AJR Am. J. Roentgenol., 126, 957-964.
2. Ciftci, A.O., Cook, R.C. and Van Velzen, D. (1996) Megacystis microcolon intestinal hypoperistalsis syndrome: evidence of a primary myocellular defect of contractile fiber synthesis. J. Pediatr. Surg., 31, 1706-1711.
3. Rolle, U., O'Briain, S., Pearl, R.H. and Puri, P. (2002) Megacystismicrocolon-intestinal hypoperistalsis syndrome: evidence of intestinal myopathy. Pediatr. Surg. Int., 18, 2-5.
4. Szigeti, R., Chumpitazi, B.P., Finegold, M.J., Ranganathan, S., Craigen, W.J., Carter, B.A. and Tatevian, N. (2010) Absent smooth muscle actin immunoreactivity of the small bowel muscularis propria circular layer in association with chromosome 15q11 deletion in megacystis-microcolon-intestinal hypoperistalsis syndrome. Pediatr. Dev. Pathol., 13, 322-325.
5. Narayanan, M., Murphy, M.S., Ainsworth, J.R. and Arul, G.S. (2007) Mydriasis in association with MMIHS in a female infant: evidence for involvement of the neuronal nicotinic acetylcholine receptor. J. Pediatr. Surg., 42, 1288-1290.
6. Richardson, C.E., Morgan, J.M., Jasani, B., Green, J.T., Rhodes, J., Williams, G.T., Lindstrom, J., Wonnacott, S., Thomas, G.A. and Smith, V. (2001) Megacystis-microcolon-intestinal hypoperistalsis syndrome and the absence of the alpha3 nicotinic acetylcholine receptor subunit. Gastroenterology, 121, 350-357.
7. Kubota, M., Ikeda, K. and Ito, Y. (1989) Autonomic innervation of the intestine from a baby with megacystis microcolon intestinal hypoperistalsis syndrome: II. Electrophysiological study. J. Pediatr. Surg., 24, 1267-1270.
8. Piaseczna Piotrowska, A., Rolle, U., Solari, V., Solari, V. and Puri, P. (2004) Interstitial cells of Cajal in the human normal urinary bladder and in the bladder of patients with megacystis-microcolon intestinal hypoperistalsis syndrome. BJU Int., 94, 143-146.
9. Piotrowska, A.P., Rolle, U., Chertin, B., De Caluwé, D., Bianchi, A. and Puri, P. (2003) Alterations in smooth muscle contractile and cytoskeleton proteins and interstitial cells of Cajal in megacystis microcolon intestinal hypoperistalsis syndrome. J. Pediatr. Surg., 38, 749-755.
10. Anneren, G., Meurling, S. and Olsen, L. (1991) Megacystismicrocolon-intestinal hypoperistalsis syndrome (MMIHS), an autosomal recessive disorder: clinical reports and review of the literature. Am. J. Med. Genet., 41, 251-254.
11. Mc Laughlin, D. and Puri, P. (2013) Familial megacystis microcolon intestinal hypoperistalsis syndrome: a systematic review. Pediatr. Surg. Int., 29, 947-951.
12. Thorson, W., Diaz-Horta, O., Foster, J., Spiliopoulos, M., Quintero, R., Farooq, A., Blanton, S. and Tekin, M. (2014) De novo ACTG2 mutations cause congenital distended bladder, microcolon, and intestinal hypoperistalsis. Hum. Genet., 133, 737-742.
13. Wangler, M.F., Gonzaga-Jauregui, C., Gambin, T., Penney, S., Moss, T., Chopra, A., Probst, F.J., Xia, F., Yang, Y., Werlin, S. et al. (2014) Heterozygous de novo and inherited mutations in the smooth muscle actin (ACTG2) gene underlie megacystis-microcolon-intestinal hypoperistalsis syndrome. PLoS Genet., 10, e1004258.
14. Tuzovic, L., Tang, S., Miller, R.S., Rohena, L., Shahmirzadi, L., Gonzalez, K., Li, X., LeDuc, C.A., Guo, J., Wilson, A. et al. (2015) New insights into the genetics of fetal megacystis: ACTG2 mutations, encoding γ-2 smooth muscle actin in megacystis microcolon intestinal hypoperistalsis syndrome (Berdon syndrome). Fetal Diagn. Ther., 38, 296-306.
15. Gauthier, J., Ouled Amar Bencheikh, B., Hamdan, F.F., Harrison, S.M., Baker, L.A., Couture, F., Thiffault, I., Ouazzani, R., Samuels, M.E., Mitchell, G.A. et al. (2014) A homozygous loss-of-function variant in MYH11 in a case with megacystismicrocolon-intestinal hypoperistalsis syndrome. Eur. J. Hum. Genet., 23, 1266-1268.
16. Miwa, T., Manabe, Y., Kurokawa, K., Kamada, S., Kanda, N., Bruns, G., Ueyama, H. and Kakunaga, T. (1991) Structure, chromosome location, and expression of the human smooth muscle (enteric type) gamma-actin gene: evolution of six human actin genes. Mol. Cell Biol., 11, 3296-3306.
17. Szucsik, J.C. and Lessard, J.L. (1995) Cloning and sequence analysis of the mouse smooth muscle gamma-enteric actin gene. Genomics, 28, 154-162.
18. Morano, I., Chai, G.X., Baltas, L.G., Lamounier-Zepter, V., Lutsch, G., Kott, M., Haase, H. and Bader, M. (2000) Smoothmuscle contraction without smooth-muscle myosin. Nat. Cell Biol., 2, 371-375.
19. Lehtonen, H.J., Sipponen, T., Tojkander, S., Karikoski, R., Järvinen, H., Laing, N.G., Lappalainen, P., Aaltonen, L.A. and Tuupanen, S. (2012) Segregation of a missense variant in enteric smooth muscle actin gamma-2 with autosomal dominant familial visceral myopathy. Gastroenterology, 143, 1482-1491.
20. Holla, O.L., Bock, G., Busk, O.L. and Isfoss, B.L. (2014) Familial visceral myopathy diagnosed by exome sequencing of a patient with chronic intestinal pseudo-obstruction. Endoscopy, 46, 533-537.
21. Klar, J., Raykova, D., Gustafson, E., Tóthová, I., Ameur, A., Wanders, A. and Dahl, N. (2015) Phenotypic expansion of visceral myopathy associated with ACTG2 tandem base substitution. Eur. J. Hum. Genet., 23, 1679-1683.
22. Arnoldi, R., Hiltbrunner, A., Dugina, V., Tille, J.C. and Chaponnier, C. (2013) Smooth muscle actin isoforms: a tug of war between contraction and compliance. Eur. J. Cell Biol., 92, 187-200.
23. Milewicz, D.M., Østergaard, J.R., Ala-Kokko, L.M., Khan, N., Grange, D.K., Mendoza-Londono, R., Bradley, T.J., Olney, A. H., Adès, L., Maher, J.F. et al. (2010) De novo ACTA2 mutation causes a novel syndrome of multisystemic smooth muscle dysfunction. Am J. Med. Genet., 152, 2437-2443.
24. Richer, J., Milewicz, D.M., Gow, R., de Nanassy, J., Maharajh, G., Miller, E., Oppenheimer, L., Weiler, G. and O'Connor, M. (2012) R179H mutation in ACTA2 expanding the phenotype to include prune-belly sequence and skin manifestations. Am. J. Med. Genet. A, 158A, 664-668.
25. Gargiulo, A., Auricchio, R., Barone, M.V., Cotugno, G., Reardon, W., Milla, P.J., Ballabio, A., Ciccodicola, A. and Auricchio, A. (2007) Filamin A is mutated in X-linked chronic idiopathic intestinal pseudo-obstruction with central nervous system involvement. Am. J. Hum. Genet., 80, 751-758.
26. Clayton-Smith, J., Walters, S., Hobson, E., Burkitt-Wright, E., Smith, R., Toutain, A., Amiel, J., Lyonnet, S., Mansour, S., Fitzpatrick, D. et al. (2008) Xq28 duplication presenting with intestinal and bladder dysfunction and a distinctive facial appearance. Eur. J. Hum. Genet., 17, 434-443.
27. Kapur, R.P., Robertson, S.P., Hannibal, M.C., Finn, L.S., Morgan, T., van Kogelenberg, M. and Loren, D.J. (2010) Diffuse abnormal layering of small intestinal smooth muscle is present in patients with FLNA mutations and x-linked intestinal pseudo-obstruction. Am. J. Surg. Pathol., 34, 1528-1543.
28. Wangler, M.F. and Beaudet, A.L. (2015) ACTG2-related disorders. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993-2015. In: Pagon, R.A., Adam, M.P., Ardinger, H.H., Wallace, S.E., Amemiya, A., Bean, L.J.H., Bird, T.D., Fong, C.T., Smith, R.J.H. and Stephens, K., editors.
29. Talisetti, A., Longacre, T., Pai, R.K. and Kerner, J. (2009) Diversion colitis in a 19-year-old female with megacystis-microcolon-intestinal hypoperistalsis syndrome. Dig. Dis. Sci., 54, 2338-2340.
30. Sasaki, K., Sakabe, K., Sakabe, N., Kondo, H. and Shimomur, M. (1993) Refined structure and solvent network of chicken gizzard G-actin DNase 1 complex at 1.8A resolution. Acta Crystallogr. Sect. A, 49, C111-C112.
31. Humphrey, W., Dalke, A. and Schulten, K. (1996) VMD-visual molecular dynamics. J. Molec. Graphics, 14, 33-38.
32. Phillips, J.C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R.D., Kalé, L. and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem., 26, 1781-1802.