A designed point mutant in fis1 disrupts dimerization and mitochondrial fission

Journal of Molecular Biology

Volumn 423, Issue 2, 2012, Pages 143-158

  Lees, Jonathan P B ^a   Manlandro, Cara Marie ^a   Picton, Lora K ^a   Tan, Alexandra Z Ebie ^b   Casares, Salvador ^a   Flanagan, John M ^c   Fleming, Karen G ^b   Hill, R Blake ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

domain swapped dimer; kinetic trap; membrane fission; mitochondria; tetratricopeptide repeat (TPR) like domains

Indexed keywords

MEMBRANE PROTEIN; PROTEIN FIS1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; COVALENT BOND; CRYSTAL STRUCTURE; CYTOSOL; DIMERIZATION; GENE MUTATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; ROOM TEMPERATURE; TETRATRICOPEPTIDE REPEAT;

SACCHAROMYCES CEREVISIAE;

EID: 84866492970     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.06.042     Document Type: Article

References (86)

1. F. Camoes, N.A. Bonekamp, H.K. Delille, and M. Schrader Organelle dynamics and dysfunction: a closer link between peroxisomes and mitochondria J. Inherit. Metab. Dis. 32 2009 163 180 10.1007/s10545-008-1018-3
2. S. Gandre-Babbe, and A.M. van der Bliek The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells Mol. Biol. Cell 19 2008 2402 2412 10.1091/mbc.E07-12-1287
3. A.M. Motley, G.P. Ward, and E.H. Hettema Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p J. Cell Sci. 121 2008 1633 1640 10.1242/jcs.026344
4. S. Kobayashi, A. Tanaka, and Y. Fujiki Fis1, DLP1, and Pex11p coordinately regulate peroxisome morphogenesis Exp. Cell Res. 313 2007 1675 1686 10.1016/j.yexcr.2007.02.028
5. T. Nguyen, J. Bjorkman, B.C. Paton, and D.I. Crane Failure of microtubule-mediated peroxisome division and trafficking in disorders with reduced peroxisome abundance J. Cell Sci. 119 2006 636 645 10.1242/jcs.02776 jcs.02776 [pii]
6. A. Koch, M. Thiemann, M. Grabenbauer, Y. Yoon, M.A. McNiven, and M. Schrader Dynamin-like protein 1 is involved in peroxisomal fission J. Biol. Chem. 278 2003 8597 8605 10.1074/jbc.M211761200 M211761200 [pii]
7. X. Li, and S.J. Gould The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11 J. Biol. Chem. 278 2003 17012 17020 10.1074/jbc.M212031200 [doi]; M212031200 [pii]
8. A. Koch, Y. Yoon, N.A. Bonekamp, M.A. McNiven, and M. Schrader A role for Fis1 in both mitochondrial and peroxisomal fission in mammalian cells Mol. Biol. Cell 16 2005 5077 5086 10.1091/mbc.E05-02-0159 E05-02-0159 [pii]
9. S. Frank Dysregulation of mitochondrial fusion and fission: an emerging concept in neurodegeneration Acta Neuropathol. (Berl) 111 2006 93 100 10.1007/s00401-005-0002-3
10. A. Santel Get the balance right: mitofusins roles in health and disease Biochim. Biophys. Acta 1763 2006 490 499 10.1016/j.bbamcr.2006.02.004 S0167-4889(06)00032-2 [pii]
11. E.A. Amiott, P. Lott, J. Soto, P.B. Kang, J.M. McCaffery, and S. Dimauro Mitochondrial fusion and function in Charcot-Marie-Tooth type 2A patient fibroblasts with mitofusin 2 mutations Exp. Neurol. 2008 10.1016/j.expneurol. 2008.01.010
12. H.R. Waterham, J. Koster, C.W. van Roermund, P.A. Mooyer, R.J. Wanders, and J.V. Leonard A lethal defect of mitochondrial and peroxisomal fission N. Engl. J. Med. 356 2007 1736 1741 10.1056/NEJMoa064436 356/17/1736 [pii]
13. D.C. Chan Mitochondrial dynamics in disease N. Engl. J. Med. 356 2007 1707
14. H. Ashrafian, L. Docherty, V. Leo, C. Towlson, M. Neilan, and V. Steeples A mutation in the mitochondrial fission gene Dnm1l leads to cardiomyopathy PLoS Genet. 6 2010 e1001000 10.1371/journal.pgen.1001000
15. E. Smirnova, D.L. Shurland, S.N. Ryazantsev, and A.M. van der Bliek A human dynamin-related protein controls the distribution of mitochondria J. Cell Biol. 143 1998 351 358
16. D. Otsuga, B.R. Keegan, E. Brisch, J.W. Thatcher, G.J. Hermann, W. Bleazard, and J.M. Shaw The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast J. Cell Biol. 143 1998 333 349
17. A.D. Mozdy, J.M. McCaffery, and J.M. Shaw Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p J. Cell Biol. 151 2000 367 380
18. Q. Tieu, and J. Nunnari Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division J. Cell Biol. 151 2000 353 366
19. P. Fekkes, K.A. Shepard, and M.P. Yaffe Gag3p, an outer membrane protein required for fission of mitochondrial tubules J. Cell Biol. 151 2000 333 340
20. Y. Yoon, E.W. Krueger, B.J. Oswald, and M.A. McNiven The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1 Mol. Cell. Biol. 23 2003 5409 5420
21. S. Jakobs, N. Martini, A.C. Schauss, A. Egner, B. Westermann, and S.W. Hell Spatial and temporal dynamics of budding yeast mitochondria lacking the division component Fis1p J. Cell Sci. 116 2003 2005 2014 10.1242/jcs.00423 jcs.00423 [pii]
22. D.I. James, P.A. Parone, Y. Mattenberger, and J.C. Martinou hFis1, a novel component of the mammalian mitochondrial fission machinery J. Biol. Chem. 278 2003 36373 36379 10.1074/jbc.M303758200 M303758200 [pii]
23. D. Stojanovski, O.S. Koutsopoulos, K. Okamoto, and M.T. Ryan Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology J. Cell Sci. 117 2004 1201 1210 10.1242/jcs.01058 117/7/1201 [pii]
24. A.C. Schauss, J. Bewersdorf, and S. Jakobs Fis1p and Caf4p, but not Mdv1p, determine the polar localization of Dnm1p clusters on the mitochondrial surface J. Cell Sci. 119 2006 3098 3106 10.1242/jcs.03026 jcs.03026 [pii]
25. R.C. Wells, L.K. Picton, S.C. Williams, F.J. Tan, and R.B. Hill Direct binding of the dynamin-like GTPase, Dnm1, to mitochondrial dynamics protein Fis1 is negatively regulated by the Fis1 N-terminal arm J. Biol. Chem. 282 2007 33769 33775 10.1074/jbc.M700807200
26. E.E. Griffin, J. Graumann, and D.C. Chan The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria J. Cell Biol. 170 2005 237 248 10.1083/jcb.200503148 jcb.200503148 [pii]
27. Y. Zhang, and D.C. Chan Structural basis for recruitment of mitochondrial fission complexes by Fis1 Proc. Natl Acad. Sci. USA 104 2007 18526 18530
28. A. Jofuku, N. Ishihara, and K. Mihara Analysis of functional domains of rat mitochondrial Fis1, the mitochondrial fission-stimulating protein Biochem. Biophys. Res. Commun. 333 2005 650 659 10.1016/j.bbrc.2005.05.154 S0006-291X(05)01103-4 [pii]
29. M.N. Serasinghe, and Y. Yoon The mitochondrial outer membrane protein hFis1 regulates mitochondrial morphology and fission through self-interaction Exp. Cell Res. 2008 10.1016/j.yexcr.2008.09.009
30. Ohashi W., Hirota H., Yamazaki T., Koshiba S., Hamada T., Yoshida M. & Yokoyama S. (2002) Solution structure of RSGI RUH-001, a Fis1p-like and CGI-135 homologous domain from a mouse cDNA.
31. M. Suzuki, S.Y. Jeong, M. Karbowski, R.J. Youle, and N. Tjandra The solution structure of human mitochondria fission protein Fis1 reveals a novel TPR-like helix bundle J. Mol. Biol. 334 2003 445 458 S002228360301221X [pii]
32. J.A. Dohm, S.J. Lee, J.M. Hardwick, R.B. Hill, and A.G. Gittis Cytosolic domain of the human mitochondrial fission protein Fis1 adopts a TPR fold Proteins 54 2004 153 156 10.1002/prot.10524
33. M. Suzuki, A. Neutzner, N. Tjandra, and R.J. Youle Novel structure of the N terminus in yeast Fis1 correlates with a specialized function in mitochondrial fission J. Biol. Chem. 280 2005 21444 21452 10.1074/jbc.M414092200 M414092200 [pii]
34. J.E. Tooley, V. Khangulov, J.P. Lees, J.L. Schlessman, M.C. Bewley, and A. Héroux 1.75 Å crystal structure of fission protein Fis1 from Saccharomyces cerevisiae reveals elusive interactions of the autoinhibitory domain Acta Crystallogr., Sect. F 67 2011 1310 1315
35. Y. Zhang, N.C. Chan, H.B. Ngo, H. Gristick, and D.C. Chan Crystal structure of mitochondrial fission complex reveals scaffolding function for mitochondrial division 1 (mdv1) coiled coil J. Biol. Chem. 287 2012 9855 9861 10.1074/jbc.M111.329359
36. L.K. Picton, S. Casares, A.C. Monahan, A. Majumdar, and R.B. Hill Evidence for conformational heterogeneity of fission protein Fis1 from Saccharomyces cerevisiae Biochemistry 48 2009 6598 6609 10.1021/bi802221h
37. DeLano, W. L. (2002). PyMOL. http://www.pymol.org.
38. M.A. Karren, E.M. Coonrod, T.K. Anderson, and J.M. Shaw The role of Fis1p-Mdv1p interactions in mitochondrial fission complex assembly J. Cell Biol. 171 2005 291 301 10.1083/jcb.200506158 jcb.200506158 [pii]
39. Q. Tieu, V. Okreglak, K. Naylor, and J. Nunnari The WD repeat protein, Mdv1p, functions as a molecular adaptor by interacting with Dnm1p and Fis1p during mitochondrial fission J. Cell Biol. 158 2002 445 452 10.1083/jcb. 200205031 jcb.200205031 [pii]
40. S. Koirala, H.T. Bui, H.L. Schubert, D.M. Eckert, C.P. Hill, M.S. Kay, and J.M. Shaw Molecular architecture of a dynamin adaptor: implications for assembly of mitochondrial fission complexes J. Cell Biol. 191 2010 1127 1139 10.1083/jcb.201005046
41. M.K. Ramarao, M.J. Bianchetta, J. Lanken, and J.B. Cohen Role of rapsyn tetratricopeptide repeat and coiled-coil domains in self-association and nicotinic acetylcholine receptor clustering J. Biol. Chem. 276 2001 7475 7483 10.1074/jbc.M009888200
42. M. Jinek, J. Rehwinkel, B.D. Lazarus, E. Izaurralde, J.A. Hanover, and E. Conti The superhelical TPR-repeat domain of O-linked GlcNAc transferase exhibits structural similarities to importin alpha Nat. Struct. Mol. Biol. 11 2004 1001 1007 10.1038/nsmb833
43. Y. Bai, T.C. Auperin, C.Y. Chou, G.G. Chang, J.L. Manley, and L. Tong Crystal structure of murine CstF-77: dimeric association and implications for polyadenylation of mRNA precursors Mol. Cell 25 2007 863 875 10.1016/j.molcel.2007.01.034
44. A. Nyarko, K. Mosbahi, A.J. Rowe, A. Leech, M. Boter, K. Shirasu, and C. Kleanthous TPR-mediated self-association of plant SGT1 Biochemistry 46 2007 11331 11341
45. D. Han, K. Kim, Y. Kim, Y. Kang, J.Y. Lee, and Y. Kim Crystal structure of the N-terminal domain of anaphase-promoting complex subunit 7 J. Biol. Chem. 284 2009 15137 15146 10.1074/jbc.M804887200
46. C. Graf, M. Stankiewicz, R. Nikolay, and M.P. Mayer Insights into the conformational dynamics of the E3 ubiquitin ligase CHIP in complex with chaperones and E2 enzymes Biochemistry 49 2010 2121 2129 10.1021/bi901829f
47. Z. Zhang, K. Kulkarni, S.J. Hanrahan, A.J. Thompson, and D. Barford The APC/C subunit Cdc16/Cut9 is a contiguous tetratricopeptide repeat superhelix with a homo-dimer interface similar to Cdc27 EMBO J. 29 2010 3733 3744 10.1038/emboj.2010.247
48. Z. Zhang, S.M. Roe, M. Diogon, E. Kong, Alaoui H. El, and D. Barford Molecular structure of the N-terminal domain of the APC/C subunit Cdc27 reveals a homo-dimeric tetratricopeptide repeat architecture J. Mol. Biol. 397 2010 1316 1328 10.1016/j.jmb.2010.02.045
49. A.M. Krachler, A. Sharma, and C. Kleanthous Self-association of TPR domains: lessons learned from a designed, consensus-based TPR oligomer Proteins 78 2010 2131 2143 10.1002/prot.22726
50. K.T. O'Neil, and W.F. DeGrado A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids Science 250 1990 646 651
51. G.J. Hermann, and J.M. Shaw Mitochondrial dynamics in yeast Annu. Rev. Cell Dev. Biol. 14 1998 265 303 10.1146/annurev.cellbio.14.1.265
52. D. Rapaport, M. Brunner, W. Neupert, and B. Westermann Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae J. Biol. Chem. 273 1998 20150 20155
53. T. Yu, R.J. Fox, L.S. Burwell, and Y. Yoon Regulation of mitochondrial fission and apoptosis by the mitochondrial outer membrane protein hFis1 J. Cell Sci. 118 2005 4141 4151 10.1242/jcs.02537 jcs.02537 [pii]
54. A. Kumar, C. Roach, I.S. Hirsh, S. Turley, S. deWalque, P.A. Michels, and W.G. Hol An unexpected extended conformation for the third TPR motif of the peroxin PEX5 from Trypanosoma brucei J. Mol. Biol. 307 2001 271 282 10.1006/jmbi.2000.4465
55. P. Sampathkumar, C. Roach, P.A. Michels, and W.G. Hol Structural insights into the recognition of peroxisomal targeting signal 1 by Trypanosoma brucei peroxin 5 J. Mol. Biol. 381 2008 867 880 10.1016/j.jmb.2008.05.089
56. P. Taylor, J. Dornan, A. Carrello, R.F. Minchin, T. Ratajczak, and M.D. Walkinshaw Two structures of cyclophilin 40: folding and fidelity in the TPR domains Structure 9 2001 431 438
57. C.J. McCleverty, L. Columbus, A. Kreusch, and S.A. Lesley Structure and ligand binding of the soluble domain of a Thermotoga maritima membrane protein of unknown function TM1634 Protein Sci. 17 2008 869 877 10.1110/ps.083432208
58. R.C. Wells, and R.B. Hill The cytosolic domain of Fis1 binds and reversibly clusters lipid vesicles PLoS One 6 2011 e21384 10.1371/journal.pone. 0021384
59. P.K. Bansal, A. Nourse, R. Abdulle, and K. Kitagawa Sgt1 dimerization is required for yeast kinetochore assembly J. Biol. Chem. 284 2009 3586 3592 10.1074/jbc.M806281200
60. R.K. Allan, and T. Ratajczak Versatile TPR domains accommodate different modes of target protein recognition and function Cell Stress Chaperones 16 2011 353 367 10.1007/s12192-010-0248-0
61. M. Bennett, M. Schlunegger, and D. Eisenberg 3d domain swapping - a mechanism for oligomer assembly Protein Sci. 4 1995 2455 2468
62. R. Fletterick, and J. Bazan When one and one are not 2 Rid B-4562-2010 Nat. Struct. Biol. 2 1995 721 723 10.1038/nsb0995-721
63. A. Saint-Jean, K. Phillips, D. Creighton, and M. Stone Active monomeric and dimeric forms of Pseudomonas putida glyoxalase I: evidence for 3D domain swapping Biochemistry (N.Y.) 37 1998 10345 10353 10.1021/bi980868q
64. J. Schymkowitz, F. Rousseau, H. Wilkinson, A. Friedler, and L. Itzhaki Observation of signal transduction in three-dimensional domain swapping Nat. Struct. Biol. 8 2001 888 892 10.1038/nsb1001-888
65. F. Rousseau, J. Schymkowitz, and L. Itzhaki The unfolding story of three-dimensional domain swapping Structure 11 2003 243 251 10.1016/S0969- 2126(03)00029-7
66. M. Czjzek, S. Letoffe, C. Wandersman, M. Delepierre, A. Lecroisey, and N. Izadi-Pruneyre The crystal structure of the secreted dimeric form of the hemophore HasA reveals a domain swapping with an exchanged heme ligand J. Mol. Biol. 365 2007 1176 1186 10.1016/j.jmb.2006.10.063
67. B. Nagar, M. Overduin, M. Ikura, and J. Rini Structural basis of calcium-induced E-cadherin rigidification and dimerization RID C-1297-2010 Nature 380 1996 360 364 10.1038/380360a0
68. J. Vendome, S. Posy, X. Jin, F. Bahna, G. Ahlsen, L. Shapiro, and B. Honig Molecular design principles underlying beta-strand swapping in the adhesive dimerization of cadherins Nat. Struct. Mol. Biol. 18 2011 693 700 10.1038/nsmb.2051
69. S.Y. Jeong, B. Gaume, Y.J. Lee, Y.T. Hsu, S.W. Ryu, S.H. Yoon, and R.J. Youle Bcl-x(L) sequesters its C-terminal membrane anchor in soluble, cytosolic homodimers EMBO J. 23 2004 2146 2155
70. J.W. O'Neill, M.K. Manion, B. Maguire, and D.M. Hockenbery BCL-XL dimerization by three-dimensional domain swapping J. Mol. Biol. 356 2006 367 381 10.1016/j.jmb.2005.11.032
71. A.Y. Denisov, T. Sprules, J. Fraser, G. Kozlov, and K. Gehring Heat-induced dimerization of BCL-xL through alpha-helix swapping Biochemistry 46 2007 734 740 10.1021/bi062080a
72. A. DeAntoni, V. Sala, and A. Musacchio Explaining the oligomerization properties of the spindle assembly checkpoint protein Mad2 Philos. Trans. R. Soc. Lond. B Biol. Sci. 360 2005 637 647 10.1098/rstb.2004.1618 discussion 447-8
73. X. Luo, and H. Yu Protein metamorphosis: the two-state behavior of Mad2 Structure 16 2008 1616 1625 10.1016/j.str.2008.10.002
74. R.L. Tuinstra, F.C. Peterson, S. Kutlesa, E.S. Elgin, M.A. Kron, and B.F. Volkman Interconversion between two unrelated protein folds in the lymphotactin native state Proc. Natl Acad. Sci. USA 105 2008 5057 5062 10.1073/pnas. 0709518105
75. A.G. Murzin Biochemistry. Metamorphic proteins Science 320 2008 1725 1726 10.1126/science.1158868
76. I. Yadid, N. Kirshenbaum, M. Sharon, O. Dym, and D.S. Tawfik Metamorphic proteins mediate evolutionary transitions of structure Proc. Natl Acad. Sci. USA 107 2010 7287 7292 10.1073/pnas.0912616107
77. K.G. Fleming, A.L. Ackerman, and D.M. Engelman The effect of point mutations on the free energy of transmembrane alpha-helix dimerization J. Mol. Biol. 272 1997 266 275
78. A.M. Stanley, P. Chuawong, T.L. Hendrickson, and K.G. Fleming Energetics of outer membrane phospholipase A (OMPLA) dimerization J. Mol. Biol. 358 2006 120 131 10.1016/j.jmb.2006.01.033
79. D.A. Yphantis Equilibrium ultracentrifugation of dilute solutions Biochemistry 3 1964 297 317
80. D. Salom, B.R. Hill, J.D. Lear, and W.F. DeGrado pH-dependent tetramerization and amantadine binding of the transmembrane helix of M2 from the influenza A virus Biochemistry 39 2000 14160 14170
81. T. Laue, B. Shah, R. Ridgeway, and S.L. Pelletier Computer-aided interpretation of analytical sedimentation data for proteins S. Harding, A.J. Rowe, J.C. Horton, Analytical Ultra-Centrifugation in Biochemistry and Polymer 1992 Royal Society of Chemistry Cambridge, UK 90 125
82. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
83. B.A. Johnson Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278 2004 313 352
84. B.A. Johnson, and R.A. Blevins NMRView: A computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994
85. C.R. Chang, C.M. Manlandro, D. Arnoult, J. Stadler, A.E. Posey, R.B. Hill, and C. Blackstone A lethal de novo mutation in the middle domain of the dynamin-related GTPase Drp1 impairs higher order assembly and mitochondrial division J. Biol. Chem. 285 2010 32494 32503 10.1074/jbc.M110.142430
86. P.P. Zhu, A. Patterson, J. Stadler, D.P. Seeburg, M. Sheng, and C. Blackstone Intra- and intermolecular domain interactions of the C-terminal GTPase effector domain of the multimeric dynamin-like GTPase Drp1 J. Biol. Chem. 279 2004 35967 35974 10.1074/jbc.M404105200 M404105200 [pii]