Hammerhead ribozyme-mediated silencing of the mutant fibrillin-1 of tight skin mouse: Insight into the functional role of mutant fibrillin-1

Experimental Cell Research

Volumn 312, Issue 9, 2006, Pages 1463-1474

  Menon, Rajesh P ^a,b   Menon, Malini R ^b   Shi Wen, Xu ^a   Renzoni, Elisabetta ^c   Bou Gharios, George ^d   Black, Carol M ^a   Abraham, David J ^a  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c ROYAL BROMPTON HOSPITAL   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Gene therapy; Hammerhead ribozyme; Microfibrils; Mutant fibrillin 1; Tight skin mouse

Indexed keywords

CALPONIN; CONNECTIVE TISSUE GROWTH FACTOR; FIBRILLIN 1; HAMMERHEAD RIBOZYME; PLASMINOGEN ACTIVATOR INHIBITOR 1; RESERPINE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 3; ACTIN BINDING PROTEIN; CALCIUM BINDING PROTEIN; CELL ADHESION MOLECULE; COLLAGEN; CYTOSKELETON PROTEIN; FIBRILLIN; FIBRONECTIN; FIBULIN 2; IMMEDIATE EARLY PROTEIN; RIBOZYME; SCLEROPROTEIN; SIGNAL PEPTIDE; TGFB1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOSKELETON; DNA MICROARRAY; DOWN REGULATION; EXTRACELLULAR MATRIX; FIBER; GENE; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; MOUSE; MYOFIBROBLAST; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA CLEAVAGE; TIGHT SKIN GENE; WESTERN BLOTTING; WILD TYPE; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; CYTOLOGY; FIBROBLAST; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOUSE MUTANT; MUTATION; PHYSIOLOGY;

ANIMALS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELL ADHESION MOLECULES; CERCOPITHECUS AETHIOPS; COLLAGEN; COS CELLS; CYTOSKELETAL PROTEINS; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; FIBRONECTINS; GENE EXPRESSION PROFILING; GENE SILENCING; IMMEDIATE-EARLY PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, MUTANT STRAINS; MICROFILAMENT PROTEINS; MUTATION; PLASMINOGEN ACTIVATOR INHIBITOR 1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, CATALYTIC; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 33746067548     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.01.011     Document Type: Article

References (66)

1. Green M.C., Sweet H.O., and Bunker L.E. Tight-skin, a new mutation of the mouse causing excessive growth of connective tissue and skeleton. Am. J. Pathol. 82 (1976) 493-512
2. Osborn T.G., Bauer N.E., Ross S.C., Moore T.L., and Zuckner J. The tight-skin mouse: physical and biochemical properties of the skin. J. Rheumatol. 10 (1983) 793-796
3. Kasturi K.N., Shibata S., Muryoi T., and Bona C.A. Tight-skin mouse an experimental model for scleroderma. Int. Rev. Immunol. 11 (1994) 253-271
4. Kasturi K., Muryoi T., Shibata S., Hatakeyama A., Murai C., Simakoshi Y., and Bona C. Functional properties and molecular characteristics of autoantibodies associated with tight skin syndrome. Ann. N. Y. Acad. Sci. 815 (1997) 253-262
5. Osborn T.G., Bashey R.I., Moore T.L., and Fischer V.W. Collagenous abnormalities in the heart of the tight-skin mouse. J. Mol. Cell Cardiol. 19 (1987) 581-587
6. Jablonska S., Schubert H., and Kikuchi I. Congenital fascial dystrophy: stiff skin syndrome-a human counterpart of the tight-skin mouse. J. Am. Acad. Dermatol. 21 (1989) 943-950
7. Szapiel S.V., Fulmer J.D., Hunninghake G.W., Elson N.A., Kawanami O., Ferrans V.J., and Crystal R.G. Hereditary emphysema in the tight-skin (Tsk/+) mouse. Am. Rev. Respir. Dis. 123 (1981) 680-685
8. Siracusa L.D., McGrath R., Ma Q., Moskow J.J., Manne J., Christner P.J., Buchberg A.M., and Jimenez S.A. A tandem duplication within the fibrillin 1 gene is associated with the mouse tight skin mutation. Genome Res. 6 (1996) 300-313
9. Charbonneau N.L., Ono R.N., Corson G.M., Keene D.R., and Sakai L.Y. Fine tuning of growth factor signals depends on fibrillin microfibril networks. Birth Defects Res., C Embryo. Today 72 (2004) 37-50
10. Hayward C., and Brock D.J. Fibrillin-1 mutations in Marfan syndrome and other type-1 fibrillinopathies. Hum. Mutat. 10 (1997) 415-423
11. Robinson P.N., Booms P., Katzke S., Ladewig M., Neumann L., Palz M., Pregla R., Tiecke F., and Rosenberg T. Mutations of FBN1 and genotype-phenotype correlations in Marfan syndrome and related fibrillinopathies. Hum. Mutat. 20 (2002) 153-161
12. Bouzeghrane F., Reinhardt D.P., Reudelhuber T.L., and Thibault G. Enhanced expression of fibrillin-1, a constituent of the myocardial extracellular matrix in fibrosis. Am. J. Physiol.: Heart Circ. Physiol. 289 (2005) H982-H991
13. Wallis D.D., Tan F.K., Kessler R., Kimball M.D., Cretoiu J.S., Arnett F.C., and Milewicz D.M. Fibrillin 1 abnormalities in dermal fibroblast cultures from first-degree relatives of patients with systemic sclerosis (scleroderma). Arthritis Rheum. 50 (2004) 329-332
14. Lemaire R., Farina G., Kissin E., Shipley J.M., Bona C., Korn J.H., and Lafyatis R. Mutant fibrillin 1 from tight skin mice increases extracellular matrix incorporation of microfibril-associated glycoprotein 2 and type I collagen. Arthritis Rheum. 50 (2004) 915-926
15. Kielty C.M., Raghunath M., Siracusa L.D., Sherratt M.J., Peters R., Shuttleworth C.A., and Jimenez S.A. The Tight skin mouse: demonstration of mutant fibrillin-1 production and assembly into abnormal microfibrils. J. Cell Biol. 140 (1998) 1159-1166
16. Gayraud B., Keene D.R., Sakai L.Y., and Ramirez F. New insights into the assembly of extracellular microfibrils from the analysis of the fibrillin 1 mutation in the tight skin mouse. J. Cell Biol. 150 (2000) 667-680
17. Cech T.R., and Bass B.L. Biological catalysis by RNA. Annu. Rev. Biochem. 55 (1986) 599-629
18. Haseloff J., and Gerlach W.L. Simple RNA enzymes with new and highly specific endoribonuclease activities. Nature 334 (1988) 585-591
19. Uhlenbeck O.C. A small catalytic oligoribonucleotide. Nature 328 (1987) 596-600
20. Citti L., and Rainaldi G. Synthetic hammerhead ribozymes as therapeutic tools to control disease genes. Curr. Gene Ther. 5 (2005) 11-24
21. Ohta Y., Kijima H., Ohkawa T., Kashani-Sabet M., and Scanlon K.J. Tissue-specific expression of an anti-ras ribozyme inhibits proliferation of human malignant melanoma cells. Nucleic Acids Res. 24 (1996) 938-942
22. Grassi G., Forlino A., and Marini J.C. Cleavage of collagen RNA transcripts by hammerhead ribozymes in vitro is mutation-specific and shows competitive binding effects. Nucleic Acids Res. 25 (1997) 3451-3458
23. LaVail M.M., Yasumura D., Matthes M.T., Drenser K.A., Flannery J.G., Lewin A.S., and Hauswirth W.W. Ribozyme rescue of photoreceptor cells in P23H transgenic rats: long-term survival and late-stage therapy. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 11488-11493
24. Dawson P.A., and Marini J.C. Hammerhead ribozymes selectively suppress mutant type I collagen mRNA in osteogenesis imperfecta fibroblasts. Nucleic Acids Res. 28 (2000) 4013-4020
25. Montgomery R.A., and Dietz H.C. Inhibition of fibrillin 1 expression using U1 snRNA as a vehicle for the presentation of antisense targeting sequence. Hum. Mol. Genet. 6 (1997) 519-525
26. Menon R.P., Gibson T.J., and Pastore A. The C terminus of fragile X mental retardation protein interacts with the multi-domain Ran-binding protein in the microtubule-organising centre. J.Mol.Biol. 343 (2004) 43-53
27. Denton C.P., Zheng B., Shiwen X., Zhang Z., Bou-Gharios G., Eberspaecher H., Black C.M., and de Crombrugghe B. Activation of a fibroblast-specific enhancer of the proalpha2(I) collagen gene in tight-skin mice. Arthritis Rheum. 44 (2001) 712-722
28. Jat P.S., and Sharp P.A. Large T antigens of simian virus 40 and polyomavirus efficiently establish primary fibroblasts. J. Virol. 59 (1986) 746-750
29. Holmes A., Abraham D.J., Sa S., Shiwen X., Black C.M., and Leask A. CTGF and SMADs, maintenance of scleroderma phenotype is independent of SMAD signaling. J. Biol. Chem. 276 (2001) 10594-10601
30. Menon R.P., Strom M., and Hughes R.C. Interaction of a novel cysteine and histidine-rich cytoplasmic protein with galectin-3 in a carbohydrate-independent manner. FEBS Lett. 470 (2000) 227-231
31. Kilpatrick M.W., Phylactou L.A., Godfrey M., Wu C.H., Wu G.Y., and Tsipouras P. Delivery of a hammerhead ribozyme specifically down-regulates the production of fibrillin-1 by cultured dermal fibroblasts. Hum. Mol. Genet. 5 (1996) 1939-1944
32. Menon R.P., and Hughes R.C. Determinants in the N-terminal domains of galectin-3 for secretion by a novel pathway circumventing the endoplasmic reticulum-Golgi complex. Eur. J. Biochem. 264 (1999) 569-576
33. Chambers R.C., Leoni P., Kaminski N., Laurent G.J., and Heller R.A. Global expression profiling of fibroblast responses to transforming growth factor-beta1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am. J. Pathol. 162 (2003) 533-546
34. Renzoni E.A., Abraham D.J., Howat S., Shi-Wen X., Sestini P., Bou-Gharios G., Wells A.U., Veeraraghavan S., Nicholson A.G., Denton C.P., Leask A., Pearson J.D., Black C.M., Welsh K.I., and du Bois R.M. Gene expression profiling reveals novel TGFbeta targets in adult lung fibroblasts. Respir. Res. 5 (2004) 24
35. Shi-Wen X., Chen Y., Denton C.P., Eastwood M., Renzoni E.A., Bou-Gharios G., Pearson J.D., Dashwood M., du Bois R.M., Black C.M., Leask A., and Abraham D.J. Endothelin-1 promotes myofibroblast induction through the ETA receptor via a rac/phosphoinositide 3-kinase/Akt-dependent pathway and is essential for the enhanced contractile phenotype of fibrotic fibroblasts. Mol. Biol. Cell 15 (2004) 2707-2719
36. Brigstock D.R. The CCN family: a new stimulus package. J. Endocrinol. 178 (2003) 169-175
37. Arthur M.J. Fibrogenesis II. Metalloproteinases and their inhibitors in liver fibrosis. Am. J. Physiol.: Gastrointest. Liver Physiol. 279 (2000) G245-G249
38. Tuan T.L., Wu H., Huang E.Y., Chong S.S., Laug W., Messadi D., Kelly P., and Le A. Increased plasminogen activator inhibitor-1 in keloid fibroblasts may account for their elevated collagen accumulation in fibrin gel cultures. Am. J. Pathol. 162 (2003) 1579-1589
39. Zuo F., Kaminski N., Eugui E., Allard J., Yakhini Z., Ben Dor A., Lollini L., Morris D., Kim Y., DeLustro B., Sheppard D., Pardo A., Selman M., and Heller R.A. Gene expression analysis reveals matrilysin as a key regulator of pulmonary fibrosis in mice and humans. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6292-6297
40. Vouret-Craviari V., Boulter E., Grall D., Matthews C., and Obberghen-Schilling E. ILK is required for the assembly of matrix-forming adhesions and capillary morphogenesis in endothelial cells. J.Cell Sci. 117 (2004) 4559-4569
41. Lemaire R., Korn J.H., Schiemann W.P., and Lafyatis R. Fibulin-2 and fibulin-5 alterations in tsk mice associated with disorganized hypodermal elastic fibers and skin tethering. J. Invest Dermatol. 123 (2004) 1063-1069
42. Angst B.D., Marcozzi C., and Magee A.I. The cadherin superfamily: diversity in form and function. J. Cell Sci. 114 (2001) 629-641
43. Iozzo R.V. The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J. Biol. Chem. 274 (1999) 18843-18846
44. Svensson L., Aszodi A., Reinholt F.P., Fassler R., Heinegard D., and Oldberg A. Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered lumican deposition in tendon. J. Biol. Chem. 274 (1999) 9636-9647
45. Ramirez F., Sakai L.Y., Dietz H.C., and Rifkin D.B. Fibrillin microfibrils: multipurpose extracellular networks in organismal physiology. Physiol. Genomics 19 (2004) 151-154
46. Bax D.V., Bernard S.E., Lomas A., Morgan A., Humphries J., Shuttleworth C.A., Humphries M.J., and Kielty C.M. Cell adhesion to fibrillin-1 molecules and microfibrils is mediated by alpha 5 beta 1 and alpha v beta 3 integrins. J. Biol. Chem. 278 (2003) 34605-34616
47. Igarashi A., Okochi H., Bradham D.M., and Grotendorst G.R. Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol. Biol. Cell 4 (1993) 637-645
48. Graness A., Giehl K., and Goppelt-Struebe M. Differential involvement of the integrin-linked kinase (ILK) in RhoA-dependent rearrangement of F-actin fibers and induction of connective tissue growth factor (CTGF). Cell Signalling 18 (2006) 433-440
49. Ramont L., Pasco S., Hornebeck W., Maquart F.X., and Monboisse J.C. Transforming growth factor-beta1 inhibits tumor growth in a mouse melanoma model by down-regulating the plasminogen activation system. Exp.Cell Res. 291 (2003) 1-10
50. Daniels J.T., Schultz G.S., Blalock T.D., Garrett Q., Grotendorst G.R., Dean N.M., and Khaw P.T. Mediation of transforming growth factor-beta(1)-stimulated matrix contraction by fibroblasts: a role for connective tissue growth factor in contractile scarring. Am. J. Pathol. 163 (2003) 2043-2052
51. Bonner J.C. Regulation of PDGF and its receptors in fibrotic diseases. Cytokine Growth Factor Rev. 15 (2004) 255-273
52. Kodera T., McGaha T.L., Phelps R., Paul W.E., and Bona C.A. Disrupting the IL-4 gene rescues mice homozygous for the tight-skin mutation from embryonic death and diminishes TGF-beta production by fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 3800-3805
53. Brinckmann J., Kim S., Wu J., Reinhardt D.P., Batmunkh C., Metzen E., Notbohm H., Bank R.A., Krieg T., and Hunzelmann N. Interleukin 4 and prolonged hypoxia induce a higher gene expression of lysyl hydroxylase 2 and an altered cross-link pattern: important pathogenetic steps in early and late stage of systemic scleroderma?. Matrix Biol. 24 (2005) 459-468
54. ng V.H., Evans L.A., Shiwen X., Fisher I.B., Rajkumar V., Abraham D.J., Black C.M., and Denton C.P. Monocyte chemoattractant protein 3 as a mediator of fibrosis: overexpression in systemic sclerosis and the type 1 tight-skin mouse. Arthritis Rheum. 48 (2003) 1979-1991
55. Baxter R.M., Crowell T.P., McCrann M.E., Frew E.M., and Gardner H. Analysis of the tight skin (Tsk1/+) mouse as a model for testing antifibrotic agents. Lab. Invest. 85 (2005) 1199-1209
56. Ramirez F., and Rifkin D.B. Cell signaling events: a view from the matrix. Matrix Biol. 22 (2003) 101-107
57. Gregory K.E., Ono R.N., Charbonneau N.L., Kuo C.L., Keene D.R., Bachinger H.P., and Sakai L.Y. The prodomain of BMP-7 targets the BMP-7 complex to the extracellular matrix. J. Biol. Chem. 280 (2005) 27970-27980
58. Sinha S., Heagerty A.M., Shuttleworth C.A., and Kielty C.M. Expression of latent TGF-beta binding proteins and association with TGF-beta 1 and fibrillin-1 following arterial injury. Cardiovasc. Res. 53 (2002) 971-983
59. Isogai Z., Ono R.N., Ushiro S., Keene D.R., Chen Y., Mazzieri R., Charbonneau N.L., Reinhardt D.P., Rifkin D.B., and Sakai L.Y. Latent transforming growth factor beta-binding protein 1 interacts with fibrillin and is a microfibril-associated protein. J. Biol. Chem. 278 (2003) 2750-2757
60. Tiedemann K., Batge B., Muller P.K., and Reinhardt D.P. Interactions of fibrillin-1 with heparin/heparan sulfate, implications for microfibrillar assembly. J. Biol. Chem. 276 (2001) 36035-36042
61. Jensen S.A., Reinhardt D.P., Gibson M.A., and Weiss A.S. Protein interaction studies of MAGP-1 with tropoelastin and fibrillin-1. J. Biol. Chem. 276 (2001) 39661-39666
62. Trask T.M., Trask B.C., Ritty T.M., Abrams W.R., Rosenbloom J., and Mecham R.P. Interaction of tropoelastin with the amino-terminal domains of fibrillin-1 and fibrillin-2 suggests a role for the fibrillins in elastic fiber assembly. J. Biol. Chem. 275 (2000) 24400-24406
63. Kassner A., Tiedemann K., Notbohm H., Ludwig T., Morgelin M., Reinhardt D.P., Chu M.L., Bruckner P., and Grassel S. Molecular structure and interaction of recombinant human type XVI collagen. J. Mol. Biol. 339 (2004) 835-853
64. Tiedemann K., Sasaki T., Gustafsson E., Gohring W., Batge B., Notbohm H., Timpl R., Wedel T., Schlotzer-Schrehardt U., and Reinhardt D.P. Microfibrils at basement membrane zones interact with perlecan via fibrillin-1. J. Biol. Chem. 280 (2005) 11404-11412
65. Isogai Z., Aspberg A., Keene D.R., Ono R.N., Reinhardt D.P., and Sakai L.Y. Versican interacts with fibrillin-1 and links extracellular microfibrils to other connective tissue networks. J. Biol. Chem. 277 (2002) 4565-4572
66. Lee S.S., Knott V., Jovanovic J., Harlos K., Grimes J.M., Choulier L., Mardon H.J., Stuart D.I., and Handford P.A. Structure of the integrin binding fragment from fibrillin-1 gives new insights into microfibril organization. Structure (Camb.) 12 (2004) 717-729