Drosophila basement membrane collagen col4a1 mutations cause severe myopathy

Matrix Biology

Volumn 31, Issue 1, 2012, Pages 29-37

  Kelemen Valkony, Ildikó ^a   Kiss, Márton ^a   Csiha, Judit ^a   Kiss, András ^a   Bircher, Urs ^a   Szidonya, János ^a   Maróy, Péter ^a   Juhász, Gábor ^c   Komonyi, Orbán ^a   Csiszár, Katalin ^b   Mink, Mátyás ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b UNIVERSITY OF HAWAII   (United States)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Drosophila; Multiple mutations; Myopathy; Type IV collagen

Indexed keywords

COLLAGEN TYPE 4; MUTANT PROTEIN;

3' UNTRANSLATED REGION; ALLELE; ARTICLE; BASEMENT MEMBRANE; CODING; COLLAGEN TYPE 4A 1 GENE; COLLAGEN TYPE 4A 2 GENE; CONTROLLED STUDY; DISEASE MODEL; DISEASE SEVERITY; DOMINANT GENE; DROSOPHILA; FEMALE STERILITY; GENE EXPRESSION; GENE LOCUS; GENETIC CODE; GENETIC COMPLEMENTATION; GENOME; HETEROZYGOTE; HOMOZYGOTE; IMMUNOHISTOCHEMISTRY; LARVA; MISSENSE MUTATION; MUSCLE CELL; MUTATIONAL ANALYSIS; MYOPATHY; NONHUMAN; OVIDUCT; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECESSIVE GENE; TRANSGENE; TRIPLE HELIX; ULTRASTRUCTURE;

ANIMALS; BASEMENT MEMBRANE; COLLAGEN TYPE IV; DISEASE MODELS, ANIMAL; DROSOPHILA; FEMALE; HETEROZYGOTE; HOMOZYGOTE; MUSCULAR DISEASES; MUTANT PROTEINS; MUTATION; PHENOTYPE;

MAMMALIA;

EID: 84855605628     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2011.09.004     Document Type: Article

References (56)

1. Alport A.C. Hereditary familial congenital haemorrhagic nephritis. Br. Med. J. 1927, 1:504-506.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215(3):403-410.
3. Van Agtmael T., Schlötzer-Schrehardt U., McKie L.G., Brownstein D.W., Lee A., Cross S.H., Sado Y., Mullins J.J., Pöschl E., Ian J., Jackson I.J. Dominant mutations of Col4a1 result in basement membrane defects which lead to anterior segment dysgenesis and glomerulopathy. Hum. Mol. Genet. 2005, 14:3161-3168.
4. Van Agtmael T., Bailey M.A., Schlötzer-Schrehardt U., Craigie E., Jackson I.J., Brownstein D.G., Megson I.L., Mullins J.J. Col4a1 mutation in mice causes defects in vascular function and low blood pressure associated with reduced red blood cell volume. Hum. Mol. Genet. 2010, 19:1119-1128.
5. Bitoun M., Maugenre S., Jeannet P.-Y., Lacene E., Ferrer X., Laforet P., Martin J.-J., Laporte J., Lochmuller H., Beggs A.H., Fardeau M., Eymard B., Romero N.B., Guicheney P. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat. Genet. 2005, 37:1207-1209.
6. Blumberg B., McKrell A.J., Olson P.F., Kurkinen M., Monson J.M., Natzle J.E., Fessler J.H. Basement membrane collagen IV and its specialized carboxyl domain are conserved in Drosophila, mouse and human. J. Biol. Chem. 1987, 262:5947-5950.
7. Blumberg B., McKrell A.J., Fessler J.H. Drosophila basement membrane collagen a1(IV). J. Biol. Chem. 1988, 263:18328-18337.
8. Borchellini C., Coulon J., Le Parco Y. The function of type IV collagen during Drosophila muscle development. Mech. Dev. 1996, 58:179-191.
9. Boutaud A., Borza D.-B., Bondar O., Gunwar S., Netzer K.-O., Singh N., Ninomiya Y., Sado Y., Noelken M.E., Hudson B.G. Type IV collagen of the glomerular basement membrane. J. Biol. Chem. 2000, 275:30716-30724.
10. Bradford M. A rapid method for the quantitation of microgramm quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
11. Breedveld G., de Coo I.F., Lequin M.H., Arts W.F.M., Heutink P., Gould D.B., John S.W.M., Oostra B., Mancini G.M.S. Novel mutations in three families confirm a major role of COL4A1 in hereditary porencephaly. J. Med. Genet. 2006, 43:490-495.
12. Bruckner-Tuderman L., Bruckner P. Genetic diseases of the extracellular matrix: more than just connective tissue disorders. J. Mol. Med. 1998, 76(3-4):226-237.
13. Burmester Th., Mink M., Pál M., Lászlóffy Zs, Lepesant J.-A., Maróy P. A genetic and molecular analysis in the 70CD region of the third chromosome of Drosophila melanogaster. Gene 2000, 246:157-167.
14. Clifford R., Schüpbach T. Molecular analysis of the drosophila EGF receptor homolog reveals that several genetically defined classes of alleles cluster in subdomains of the receptor protein. Genetics 1994, 137:531-550.
15. Deák P., Omar M.M., Saunders R.D.C., Pál M., Komonyi O., Szidonya J., Maróy P., Zhang Y., Ashburner M., Benos P., Savakis C., Siden-Kiamos I., Louis C., Bolshakov V., Kafatos N., Madueno F.C., Modolell E., Glover D.M. P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster. Genetics 1997, 147:1697-1722.
16. Dowling J.J., Vreede A.P., Low S.E., Gibbs E.M., Kuwada J.Y., Bonnemann C.G., Feldman E.L. Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet. 2009, 5:e1000372.
17. Favor J., Gloeckner Ch.J., Janik D., Klempt M., Neuhäuser-Klaus A., Pretsch W., Schmahl W., Quintanilla-Fend L. Type IV procollagen missense mutations associated with defects of the eye, vascular stability, the brain, kidney function and embryonic or postnatal viability in the mouse, mus musculus: an extension of the Col4a1 allelic series and the identification of the first two Col4a2 mutant alleles. Genetics 2007, 175:725-736.
18. Fessler J.H., Fessler L.I. Drosophila extrarcellular matrix. Annu. Rev. Cell Biol. 1989, 5:309-339.
19. Fessler L.I., Condic M.L., Nelson R.E., Fessler J.H., Friström J.W. Site-specific cleavage of basement membrane collagen IV during Drosophila metamorphosis. Development 1993, 117:1061-1069.
20. Glise B., Bourbon H., Noselli S. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 1995, 83:451-461.
21. Gould D.B., Phalan F.C., Breedveld G.J., van Mil S.E., Smith R.S., Schimenti J.C., Aguglia U., van der Knaap M.S., Heutink P., John S.W.M. Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science 2005, 308:1167-1171.
22. Gould D.B.F., Phalan F.C., van Mil S.E., Sundberg J.P., Vahedi K., Massin P., Bousser M.G., Heutink P., Miner J.H., Tournier-Lasserve E., John S.W.M. Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N. Engl. J. Med. 2006, 354:1489-1496.
23. Gupta M.C., Graham P.L., Kramer J.M. Characterization of 1(IV) collagen mutations in Caenorhabditis elegans and the effects of α1 and α2(IV) mutations on type IV collagen distribution. J. Cell Biol. 1997, 137:1185-1196.
24. Hynes R.O., Zhao Q. The evolution of cell adhesion. J. Cell Biol. 2000, 150:89-96.
25. Jeannet P.-Y., Bassez G., Eymard B., Laforêt P., Urtizberea J.A., Rouche A., Guicheney P., Fardeau M., Romero N.B. Clinical and histologic findings in autosomal centronuclear myopathy. Neurology 2004, 62:1484-1490.
26. Kashtan C.E. Alport syndrome. Medicine 1999, 78:338-360.
27. Kashtan C.E. Alport syndromes: phenotypic heterogeneity of progressive hereditary nephritis. Pediatr. Nephrol. 2000, 14(6):502-512.
28. Komonyi O., Mink M., Csiha J., Maróy P. Genomic organization of DHR38 gene in Drosophila: presence of Alu-like repeat in translated exon and expression during embryonic development. Arch. Insect Biochem. Physiol. 1998, 38:185-192.
29. Labelle-Dumais C., Dilworth D.J., Harrington E.P., de Leau M., Lyons D., Kabaeva Zh., Manzini M.C., Dobyns W.B., Walsh Ch.A., Michele D.E., Gould D.B. COL4A1 mutations cause ocular dysgenesis, neuronal localization defects, and myopathy in mice and Walker-Warburg syndrome in humans. PLoS Genet. 2011, 7(5):e1002062.
30. Leventis P.A., Chow B.M., Stewart B.A., Iyengar B., Campos A.R., Boulianne G.L. Drosophila Amphiphysin is a post-synaptic protein required for normal locomotion but not endocytosis. Traffic 2001, 2(11):839-850.
31. Masur S.K., Kim Y.T., Wu C.F. Reversible inhibition of endocytosis in cultured neurons from the Drosophila temperature-sensitive mutant shibirets1. J. Neurogenet. 1990, 6(3):191-206.
32. Mayer U., Saher G., Fässler R., Bornemann A., Echtermeyer F., von der Mark H., Miosge N., Pöschl E., von der Mark K. Absence of integrin alpha-7 causes a novel form of muscular dystrophy. Nat. Genet. 1997, 17:318-323.
33. Middleton C.A., Nongthomba U., Parry K., Sweeney S.T., Sparrow J.C., Elliott C.J. Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary. BMC Biol. 2006, 4:17-21.
34. Miosge N. The ultrastructural composition of basement membranes in vivo. Histol. Histopathol. 2001, 16(4):1239-1248.
35. Molnar J., Ujfaludi Z., Sheri F.T., Fong S.T.F., Bollinger J.A., Waro G., Fogelgren B., Dooley D.M., Mink M., Katalin Csiszar K. Drosophila lysyl oxidases Dmloxl-1 and Dmloxl-2 are differentially expressed and the active DmLOXL-1 influences gene expression and development. J. Biol. Chem. 2005, 280:22977-22985.
36. Monson J.M., Natzle J., Friedman J., McCarthy B.J. Expression and novel structure of a collagen gene in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 1982, 79:1761-1765.
37. Nicot A.-S., Toussaint A., Tosch V., Kretz Ch., Wallgren-Pettersson C., Iwarsson E., Kingston H., Garnier J.-M., Biancalana V., Oldfors A., Mandel J.-L., Laporte J. Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat. Genet. 2007, 39:1134-1139.
38. Ortega N., Werb Z. New functional roles for non-collagenous domains of basement membrane collagens. J. Cell Sci. 2002, 115:4201-4214.
39. Plaisier E., Gribouval O., Alamowitch S., Mougenot B., Prost C., Verpont M.Ch., Marro B., Desmettre Th., Cohen S.Y., Roullet E., Dracon M., Fardeau M., Van Agtmael T., Kerjaschki D., Antignac C., Ronco P. COL4A1 mutations and hereditary angiopathy, nephropathy, aneurysms, and muscle cramps. N. Engl. J. Med. 2007, 357:2687-2695.
40. Pöschl E., Schlötzer-Schrehardt U., Brachvogel B., Saito K., Ninomiya Y., Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 2004, 131:1619-1628.
41. Razzaq A., Robinson I.M., McMahon H.T., Skepper J.N., Su Y., Zelhof A.C., Jackson A.P., Gay N.J., O'Kane C.J. Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes Dev. 2001, 15(22):2967-2979.
42. Rheault M.N., Kren S.M., Thielen B.K., Mesa A.H.A., Crosson J.T., Thomas W., Sado Y., Kashtan C.E., Segal Y. Mouse model of X-linked Alport syndrome. J. Am. Soc. Nephrol. 2004, 15:1466-1474.
43. Rodriguez A.Z., Tang Zh.M.L., Meller S., Chen J., Bellen H., Kimbrell D.A. Identification of immune system and response genes, and novel mutations causing melanotic tumor formation in Drosophila melanogaster. Genetics 1996, 143:929-940.
44. Sado Y., Kagawa M., Naito I., Ueki Y., Seki T., Momota R., Oohashi T., Ninomiya Y. Organization and expression of basement membrane collagen IV genes and their roles in human disorders. J. Biochem. 1998, 123(5):767-776.
45. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: a Laboratory Manual 1989, Cold Spring Harbor Laboratory, Cold Spring Harbor. 2nd ed.
46. Sanes J.R. The basement membrane/basal lamina of skeletal muscle. J. Biol. Chem. 2003, 278:12601-12604.
47. Sempere L.F., Sokol N.S., Dubrovsky E.B., Berger E.M., Ambros V. Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-complex gene activity. Dev. Biol. 2003, 259:9-18.
48. Suzuki D.T. Temperature-sensitive mutations in Drosophila melanogaster. Science 1970, 170:695-706.
49. Suzuki D.T., Procunier D. Temperature-sensitive mutations in Drosophila melanogaster, III. Dominant lethals and semilethals on chromosome 2. Proc. Natl. Acad. Sci U. S. A. 1969, 62:369-376.
50. Szidonya J., Reuter G. Cytogenetic analysis of the echinoid (ed), dumpy (dp) and clot (cl) region in Drosophila melanogaster. Genet. Res. Camb. 1988, 51:197-208.
51. Szidonya J., Farkas T., Pali T. The fatty acid constitution and ordering state of membranes in dominant temperature-sensitive lethal mutation and wild-type Drosophila melanogaster larvae. Biochem. Genet. 1990, 28(5-6):233-246.
52. Tosch V., Rohde H.M., Tronchere H., Zanoteli E., Monroy N., Kretz C., Dondaine N., Payrastre B., Mandel J.-L., Laporte J. A novel PtdIns3P and PtdIns(3,5)P2 phosphatase with an inactivating variant in centronuclear myopathy. Hum. Mol. Genet. 2006, 15:3098-3106.
53. Török T., Tick G., Alvarado M., Kiss I. P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics 1993, 135:71-80.
54. Tryggvason K., Zhou J., Hostikka S.L., Shows T.B. Molecular genetics of Alport syndrome. Kidney Int. 1993, 43(1):38-44.
55. Vahedi K., Kubis N., Boukobza M., Arnoult M., Massin P., Tournier-Lasserve E., Bousser M.G. COL4A1 mutation in a patient with sporadic, recurrent intracerebral hemorrhage. Stroke 2007, 38:1461-1464.
56. Yasothornsrikul S., Davis W.J., Cramer G., Kimbrell D.A., Dearolf C.R. Viking: identification and characterization of a second type IV collagen in Drosophila. Gene 1997, 198:17-25.