DOI: 10.1146/annurev.biophys.35.040405.101953. CRYO-ELECTRON MICROSCOPY OF SPLICEOSOMAL COMPONENTS

CRYO-ELECTRON MICROSCOPY OF SPLICEOSOMAL COMPONENTS

10.1146/annurev.biophys.35.040405.101953

Crossref journal-article

Annual Reviews

Annual Review of Biophysics and Biomolecular Structure (22)

Abstract

Splicing is an essential step of gene expression in which introns are removed from pre-mRNA to generate mature mRNA that can be translated by the ribosome. This reaction is catalyzed by a large and dynamic macromolecular RNP complex called the spliceosome. The spliceosome is formed by the stepwise integration of five snRNPs composed of U1, U2, U4, U5, and U6 snRNAs and more than 150 proteins binding sequentially to pre-mRNA. To study the structure of this particularly dynamic RNP machine that undergoes many changes in composition and conformation, single-particle cryo-electron microscopy (cryo-EM) is currently the method of choice. In this review, we present the results of these cryo-EM studies along with some new perspectives on structural and functional aspects of splicing, and we outline the perspectives and limitations of the cryo-EM technique in obtaining structural information about macromolecular complexes, such as the spliceosome, involved in splicing.

Bibliography

Stark, H., & LÃ¼hrmann, R. (2006). CRYO-ELECTRON MICROSCOPY OF SPLICEOSOMAL COMPONENTS. Annual Review of Biophysics and Biomolecular Structure, 35(1), 435â457.

Authors 2

Holger Stark (first)
Reinhard Lührmann (additional)

References 101 Referenced 74

10.1016/S0968-4328(97)00068-1
10.1038/308032a0
10.1006/jmbi.1996.0171
10.1016/j.molcel.2004.07.022
10.1038/nsmb761
10.1016/S0014-5793(99)01475-1
10.1016/S0076-6879(97)77021-6
Burge C, Tuschl T, Sharp PA. 1999. Splicing of Precursors to mRNA by the Spliceosomes. Cold Spring Harbor, NY: Cold Spring Harbor Press. 525pp.
10.1006/jmbi.2002.5438
10.1101/gad.8.16.1974
10.1038/20367
10.1016/j.molcel.2005.03.021
10.1002/j.1460-2075.1993.tb05775.x
10.1126/science.8146658
10.1006/jsbi.1996.0030
10.1016/0022-2836(82)90282-0
10.1038/376441a0
10.1101/gad.13.7.851
10.1126/science.1084155
10.1016/j.molcel.2005.02.016
10.1101/gad.10.2.233
10.1016/S0168-9525(00)02176-4
10.1006/jmbi.1998.1668
10.1016/S0092-8674(00)80963-0
{'key': 'B25', 'first-page': '146', 'volume': '73', 'author': 'Harauz G', 'year': '1986', 'journal-title': 'Optik'} / Optik by Harauz G (1986)
10.1073/pnas.262483899
10.1017/S003358350000305X
10.1016/j.sbi.2005.08.004
10.1017/S1355838202021088
10.1016/S1097-2765(03)00270-3
10.1038/nsmb728
10.1016/S0959-440X(99)80032-3
10.1016/S0092-8674(00)80550-4
10.1083/jcb.145.7.1355
10.1093/nar/18.13.3803
10.1006/jsbi.1999.4174
10.1101/gad.8.24.3008
10.1126/science.1077783
10.1038/sj.emboj.7600241
10.1016/S1097-2765(01)00167-8
10.1146/annurev.bi.64.070195.002251
10.1016/S1047-8477(03)00069-8
{'key': 'B43', 'first-page': '303', 'volume-title': 'The RNA World', 'author': 'Moore MJ', 'year': '1993'} / The RNA World by Moore MJ (1993)
10.1006/jmbi.1998.2078
10.1016/j.jmb.2004.04.078
10.1038/348515a0
10.1002/j.1460-2075.1994.tb06729.x
10.1038/1700
10.1016/0092-8674(94)90563-0
10.1006/jmbi.1997.1182
10.1038/nrm1259
10.1016/0304-3991(92)90233-A
10.1016/0304-3991(94)90038-8
10.1364/JOSAA.21.000499
10.1016/j.jsb.2003.09.030
10.1038/29234
10.1002/j.1460-2075.1996.tb00481.x
10.1002/jemt.1060090405
10.1016/S1047-8477(02)00541-5
10.1101/gr.473902
10.1074/jbc.275.11.7439
10.1016/S0022-2836(03)00684-3
10.1006/jmbi.1999.3258
10.1016/j.jsb.2003.11.007
10.1093/nar/18.24.7373
10.1016/S1047-8477(03)00072-8
10.1016/j.jsb.2005.04.004
10.1038/35059098
10.1016/0968-4328(96)00018-2
10.1006/jsbi.1998.4014
10.1038/sj.emboj.7600102
10.1073/pnas.83.18.6721
10.1128/MCB.14.5.2994
10.1016/S0092-8674(00)80925-3
10.1038/35054102
10.1016/S0969-2126(01)00216-7
{'key': 'B77', 'first-page': '849', 'volume': '9', 'author': 'Stark H', 'year': '2002', 'journal-title': 'Nat. Struct. Biol.'} / Nat. Struct. Biol. by Stark H (2002)
10.1016/S0092-8674(00)81057-0
10.1074/jbc.M207685200
10.1093/emboj/20.9.2293
10.1093/emboj/20.1.187
10.1016/0304-3991(84)90066-4
10.1016/0304-3991(87)90010-6
10.1016/0304-3991(81)90059-0
10.1017/S0033583500003644
10.1006/jsbi.1996.0004
10.1002/j.1460-2075.1985.tb03944.x
10.1016/S0092-8674(00)80774-6
10.1016/S1097-2765(00)00131-3
10.1016/j.jsb.2003.11.026
10.1017/S135583829898030X
10.1101/gad.12.10.1409
10.1016/S0955-0674(97)80003-8
Will CL, Luhrmann R. 2005. Richness of RNA roles in modern RNA world. InRNA World, ed.RF Gesteland, TR Cech, JF Atkins, pp.369–400. Cold Spring Harbor, NY: Cold Spring Harbor Press. 3rd ed.
10.1515/BC.2005.084
10.1002/9783527619504.ch42
10.1093/emboj/20.16.4536
10.1093/emboj/cdf480
10.1038/nature01031
10.1006/jsbi.1996.0033
10.1073/pnas.0508048103

Dates

Type	When
Created	19 years, 4 months ago (April 7, 2006, 10:20 a.m.)
Deposited	3 years, 10 months ago (Oct. 6, 2021, 5:41 p.m.)
Indexed	1 year ago (Aug. 4, 2024, 6:41 p.m.)
Issued	19 years, 2 months ago (June 1, 2006)
Published	19 years, 2 months ago (June 1, 2006)
Published Print	19 years, 2 months ago (June 1, 2006)

Funders 0

None

BibTeX

@article{Stark_2006, title={CRYO-ELECTRON MICROSCOPY OF SPLICEOSOMAL COMPONENTS}, volume={35}, ISSN={1545-4266}, url={http://dx.doi.org/10.1146/annurev.biophys.35.040405.101953}, DOI={10.1146/annurev.biophys.35.040405.101953}, number={1}, journal={Annual Review of Biophysics and Biomolecular Structure}, publisher={Annual Reviews}, author={Stark, Holger and Lührmann, Reinhard}, year={2006}, month=jun, pages={435–457} }

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