The Impairment of MAGMAS Function in Human Is Responsible for a Severe Skeletal Dysplasia

PLoS Genetics

Volumn 10, Issue 5, 2014, Pages

  Mehawej, Cybel ^a,b   Delahodde, Agnès ^c   Legeai Mallet, Laurence ^b   Delague, Valérie ^d,e   Kaci, Nabil ^b   Desvignes, Jean Pierre ^d,e   Kibar, Zoha ^f,g   Capo Chichi, José Mario ^f,g   Chouery, Eliane ^a   Munnich, Arnold ^b   Cormier Daire, Valérie ^b   Mégarbané, André ^a  

^a SAINT JOSEPH UNIVERSITY   (Lebanon)

^b IMAGINE INSTITUTE   (France)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^d INSERM   (France)

^e AIX MARSEILLE UNIVERSITY   (France)

^f UNIVERSITY OF MONTREAL   (Canada)

^g UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MAGMAS PROTEIN; MITOCHONDRIAL PROTEIN; UNCLASSIFIED DRUG; MAGMAS PROTEIN, HUMAN; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; BONE DYSPLASIA; CARTILAGE; CASE REPORT; CELL DEATH; CHILD; CONTROLLED STUDY; EMBRYO; EXOME; GENE; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; HOMOZYGOSITY; HUMAN; HUMAN CELL; INFANT; MAGMAS GENE; MISSENSE MUTATION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRESCHOOL CHILD; PROTEIN TRANSPORT; SPONDYLODYSPLASTIC DYSPLASIA; TRABECULAR BONE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; MALE; MOLECULAR GENETICS; PEDIGREE; PHYSIOLOGY; RADIOGRAPHY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BONE DISEASES, DEVELOPMENTAL; EXOME; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PEDIGREE; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84901599269     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004311     Document Type: Article

References (42)

1. Karsenty G, Kronenberg HM, Settembre C, (2009) Genetic control of bone formation. Annu Rev Cell Dev Biol 25: 629-648 doi:10.1146/annurev.cellbio.042308.113308.
2. Baitner AC, Maurer SG, Gruen MB, Di Cesare PE, (2000) The genetic basis of the osteochondrodysplasias. J Pediatr Orthop 20: 594-605.
3. Warman ML, Cormier-Daire V, Hall C, Krakow D, Lachman R, et al. (2011) Nosology and classification of genetic skeletal disorders: 2010 revision. Am J Med Genet A 155A: 943-968 doi:10.1002/ajmg.a.33909.
4. Ikegawa S, (2006) Genetic analysis of skeletal dysplasia: recent advances and perspectives in the post-genome-sequence era. J Hum Genet 51: 581-586 doi:10.1007/s10038-006-0401-x.
5. Huber C, Faqeih EA, Bartholdi D, Bole-Feysot C, Borochowitz Z, et al. (2013) Exome sequencing identifies INPPL1 mutations as a cause of opsismodysplasia. Am J Hum Genet 92: 144-149 doi:10.1016/j.ajhg.2012.11.015.
6. Mégarbané A, Dagher R, Melki I, (2008) Sib pair with previously unreported skeletal dysplasia. Am J Med Genet A 146A: 2916-2919 doi:10.1002/ajmg.a.32540.
7. Mégarbané A, Mehawej C, El Zahr A, Haddad S, Cormier-Daire V, (2013) A Second Family with Autosomal Recessive Spondylometaphyseal Dysplasia and Early Death. Am J Med Genet A 164: 1010-4 doi:10.1002/ajmg.a.36372.
8. Lander ES, Botstein D, (1987) Homozygosity mapping: a way to map human recessive traits with the DNA of inbred children. Science 236: 1567-1570.
9. Kumar P, Henikoff S, Ng PC, (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081 doi:10.1038/nprot.2009.86.
10. Choi Y, Sims GE, Murphy S, Miller JR, Chan AP, (2012) Predicting the functional effect of amino acid substitutions and indels. PloS One 7: e46688 doi:10.1371/journal.pone.0046688.
11. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575 doi:10.1086/519795.
12. Frazier AE, Dudek J, Guiard B, Voos W, Li Y, et al. (2004) Pam16 has an essential role in the mitochondrial protein import motor. Nat Struct Mol Biol 11: 226-233 doi:10.1038/nsmb735.
13. Jubinsky PT, Messer A, Bender J, Morris RE, Ciraolo GM, et al. (2001) Identification and characterization of Magmas, a novel mitochondria-associated protein involved in granulocyte-macrophage colony-stimulating factor signal transduction. Exp Hematol 29: 1392-1402.
14. Peng J, Huang C-H, Short MK, Jubinsky PT, (2005) Magmas gene structure and evolution. In Silico Biol 5: 251-263.
15. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
16. Becker S, Gehrsitz A, Bork P, Buchner S, Buchner E, (2001) The black-pearl gene of Drosophila defines a novel conserved protein family and is required for larval growth and survival. Gene 262: 15-22 doi:10.1016/S0378-1119(00)00548-5.
17. Sinha D, Joshi N, Chittoor B, Samji P, D'Silva P, (2010) Role of Magmas in protein transport and human mitochondria biogenesis. Hum Mol Genet 19: 1248-1262 doi:10.1093/hmg/ddq002.
18. Schatz G, Dobberstein B, (1996) Common principles of protein translocation across membranes. Science 271: 1519-1526.
19. Wagner K, Mick DU, Rehling P, (2009) Protein transport machineries for precursor translocation across the inner mitochondrial membrane. Biochim Biophys Acta 1793: 52-59 doi:10.1016/j.bbamcr.2008.05.026.
20. Roy S, Short MK, Stanley ER, Jubinsky PT, (2012) Essential role of Drosophila black-pearl is mediated by its effects on mitochondrial respiration. FASEB J Off Publ Fed Am Soc Exp Biol 26: 3822-3833 doi:10.1096/fj.11-193540.
21. Short MK, Hallett JP, Tar K, Dange T, Schmidt M, et al. (2012) The yeast magmas ortholog pam16 has an essential function in fermentative growth that involves sphingolipid metabolism. PloS One 7: e39428 doi:10.1371/journal.pone.0039428.
22. Jubinsky PT, Short MK, Mutema G, Witte DP, (2003) Developmental expression of Magmas in murine tissues and its co-expression with the GM-CSF receptor. J Histochem Cytochem Off J Histochem Soc 51: 585-596.
23. D'Silva PR, Schilke B, Walter W, Craig EA, (2005) Role of Pam16's degenerate J domain in protein import across the mitochondrial inner membrane. Proc Natl Acad Sci U S A 102: 12419-12424 doi:10.1073/pnas.0505969102.
24. Elsner S, Simian D, Iosefson O, Marom M, Azem A, (2009) The mitochondrial protein translocation motor: Structural conservation between the human and yeast Tim14/Pam18-Tim16/Pam16 co-chaperones. Int J Mol Sci 10: 2041-2053 doi:10.3390/ijms10052041.
25. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N, (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644 doi:10.1016/j.cell.2009.08.005.
26. Sparkes R, Patton D, Bernier F, (2007) Cardiac features of a novel autosomal recessive dilated cardiomyopathic syndrome due to defective importation of mitochondrial protein. Cardiol Young 17: 215-217 doi:10.1017/S1047951107000042.
27. Davey KM, Parboosingh JS, McLeod DR, Chan A, Casey R, et al. (2006) Mutation of DNAJC19, a human homologue of yeast inner mitochondrial membrane co-chaperones, causes DCMA syndrome, a novel autosomal recessive Barth syndrome-like condition. J Med Genet 43: 385-393 doi:10.1136/jmg.2005.036657.
28. D'Silva PR, Schilke B, Hayashi M, Craig EA, (2007) Interaction of the J-Protein Heterodimer Pam18/Pam16 of the Mitochondrial Import Motor with the Translocon of the Inner Membrane. Mol Biol Cell 19: 424-432 doi:10.1091/mbc.E07-08-0748.
29. Thiel CT, Horn D, Zabel B, Ekici AB, Salinas K, et al. (2005) Severely incapacitating mutations in patients with extreme short stature identify RNA-processing endoribonuclease RMRP as an essential cell growth regulator. Am J Hum Genet 77: 795-806 doi:10.1086/497708.
30. Ridanpää M, van Eenennaam H, Pelin K, Chadwick R, Johnson C, et al. (2001) Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia. Cell 104: 195-203.
31. Bonafé L, Schmitt K, Eich G, Giedion A, Superti-Furga A, (2002) RMRP gene sequence analysis confirms a cartilage-hair hypoplasia variant with only skeletal manifestations and reveals a high density of single-nucleotide polymorphisms. Clin Genet 61: 146-151.
32. Lu Q, Wierzbicki S, Krasilnikov AS, Schmitt ME, (2010) Comparison of mitochondrial and nucleolar RNase MRP reveals identical RNA components with distinct enzymatic activities and protein components. RNA N Y N 16: 529-537 doi:10.1261/rna.1893710.
33. Glazov EA, Zankl A, Donskoi M, Kenna TJ, Thomas GP, et al. (2011) Whole-exome re-sequencing in a family quartet identifies POP1 mutations as the cause of a novel skeletal dysplasia. PLoS Genet 7: e1002027 doi:10.1371/journal.pgen.1002027.
34. Miller SA, Dykes DD, Polesky HF, (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16: 1215.
35. Sulonen A-M, Ellonen P, Almusa H, Lepistö M, Eldfors S, et al. (2011) Comparison of solution-based exome capture methods for next generation sequencing. Genome Biol 12: R94 doi:10.1186/gb-2011-12-9-r94.
36. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinforma Oxf Engl 25: 1754-1760 doi:10.1093/bioinformatics/btp324.
37. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297-1303 doi:10.1101/gr.107524.110.
38. Wang K, Li M, Hakonarson H, (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38: e164 doi:10.1093/nar/gkq603.
39. Schiestl RH, Gietz RD, (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet 16: 339-346.
40. Sikorski RS, Boeke JD, (1991) In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Methods Enzymol 194: 302-318.
41. Westermann B, Neupert W, (2000) Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 16: 1421-1427 doi:10.1002/1097-0061(200011)16:15<1421::AID-YEA624>3.0.CO;2-U.
42. Kuravi K, Nagotu S, Krikken AM, Sjollema K, Deckers M, et al. (2006) Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J Cell Sci 119: 3994-4001 doi:10.1242/jcs.03166.