AAA+ ATPases: Achieving diversity of function with conserved machinery

Traffic

Volumn 8, Issue 12, 2007, Pages 1657-1667

  White, Susan Roehl ^a   Lauring, Brett ^a  

^a Columbia University ^*  (United States)

Author keywords

AAA ATPase; Clp proteins; Dynein; P97 VCP; Pore loop; Spastin

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DYNEIN ADENOSINE TRIPHOSPHATASE; MOLECULAR MOTOR; PROTEIN P97; SPASTIN;

AUTOSOMAL RECESSIVE DISORDER; CELL FUNCTION; CELL MIGRATION; CELL TRANSPORT; COMPLEX III DEFICIENCY; GENE MUTATION; GENETIC CONSERVATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; KARTAGENER SYNDROME; MICROTUBULE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; QUALITY CONTROL; REVIEW; TORSION DYSTONIA; ZELLWEGER SYNDROME;

ADENOSINE TRIPHOSPHATASES; AMINO ACID MOTIFS; ANIMALS; BINDING SITES; CELL MEMBRANE; CONSERVED SEQUENCE; HUMANS; HYDROLYSIS; MICROTUBULES; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; MUTATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY;

EID: 35948947822     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00642.x     Document Type: Review

References (89)

1. Smith GR, Contreras-Moreira B, Zhang X, Bates PA. A link between sequence conservation and domain motion within the AAA+ family. J Struct Biol 2004; 146: 189-204.
2. Wang J, Song JJ, Franklin MC, Kamtekar S, Im YJ, Rho SH, Seong IS, Lee CS, Chung CH, Eom SH. Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure 2001; 9: 177-184.
3. Yamada-Inagawa T, Okuno T, Karata K, Yamanaka K, Ogura T. Conserved pore residues in the AAA protease FtsH are important for proteolysis and its coupling to ATP hydrolysis. J Biol Chem 2003; 278: 50182-50187.
4. Siddiqui SM, Sauer RT, Baker TA. Role of the processing pore of the ClpX AAA+ ATPase in the recognition and engagement of specific protein substrates. Genes Dev 2004; 18: 369-374.
5. Lum R, Tkach JM, Vierling E, Glover JR. Evidence for an unfolding/ threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J Biol Chem 2004; 279: 29139-29146.
6. Schlieker C, Weibezahn J, Patzelt H, Tessarz P, Strub C, Zeth K, Erbse A, Schneider-Mergener J, Chin JW, Schultz PG, Bukau B, Mogk A. Substrate recognition by the AAA+ chaperone ClpB. Nat Struct Mol Biol 2004; 11: 607-615.
7. Hanson PI, Whiteheart SW. AAA+ proteins: Have engine, will work. Nat Rev Mol Cell Biol 2005; 6: 519-529.
8. Neuwald AF, Aravind L, Spouge JL, Koonin EV. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 1999; 9: 27-43.
9. Lupas AN, Martin J. AAA proteins. Curr Opin Struct Biol 2002; 12: 746-753.
10. Tomoyasu T, Yuki T, Morimura S, Mori H, Yamanaka K, Niki H, Hiraga S, Ogura T. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J Bacteriol 1993; 175: 1344-1351.
11. Iyer LM, Leipe DD, Koonin EV, Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 2004; 146: 11-31.
12. Hattendorf DA, Lindquist SL. Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J 2002; 21: 12-21.
13. DeLaBarre B, Christianson JC, Kopito RR, Brunger AT. Central pore residues mediate the p97/VCP activity required for ERAD. Mol Cell 2006; 22: 451-462.
14. Block MR, Glick BS, Wilcox CA, Wieland FT, Rothman JE. Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc Natl Acad Sci U S A 1988; 85: 7852-7856.
15. Ungermann C, Nichols BJ, Pelham HR, Wickner W. A vacuolar v-t-SNARE complex, the predominant form in vivo and on isolated vacuoles, is disassembled and activated for docking and fusion. J Cell Biol 1998; 140: 61-69.
16. Babst M, Wendland B, Estepa EJ, Emr SD. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 1998; 17: 2982-2993.
17. Platta HW, Grunau S, Rosenkranz K, Girzalsky W, Erdmann R. Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol. Nat Cell Biol 2005; 7: 817-822.
18. Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, Bukau B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 1999; 96: 13732-13737.
19. Hoskins JR, Pak M, Maurizi MR, Wickner S. The role of the ClpA chaperone in proteolysis by ClpAP. Proc Natl Acad Sci U S A 1998; 95: 12135-12140.
20. Kim YI, Burton RE, Burton BM, Sauer RT, Baker TA. Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol Cell 2000; 5: 639-648.
21. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, Cjeka Z, Baumeister W, Fried VA, Finley D. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 1998; 94: 615-623.
22. Banfi S, Bassi MT, Andolfi G, Marchitiello A, Zanotta S, Ballabio A, Casari G, Franco B. Identification and characterization of AFG3L2, a novel paraplegin-related gene. Genomics 1999; 59: 51-58.
23. Casari G, De Fusco M, Ciarmatori S, Zeviani M, Mora M, Fernandez P, De Michele G, Filla A, Cocozza S, Marconi R, Durr A, Fontaine B, Ballabio A. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 1998; 93: 973-983.
24. Ishihara N, Fujita Y, Oka T, Mihara K. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J 2006; 25: 2966-2977.
25. Tatsuta T, Augustin S, Nolden M, Friedrichs B, Langer T. m-AAA protease-driven membrane dislocation allows intramembrane cleavage by rhomboid in mitochondria. EMBO J 2007; 26: 325-335.
26. Coppola M, Pizzigoni A, Banfi S, Bassi MT, Casari G, Incerti B. Identification and characterization of YME1L1, a novel paraplegin-related gene. Genomics 2000; 66: 48-54.
27. Rainey RN, Glavin JD, Chen HW, French SW, Teitell MA, Koehler CM. A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space. Mol Cell Biol 2006; 26: 8488-8497.
28. Ye Y, Meyer HH, Rapoport TA. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 2001; 414: 652-656.
29. Latterich M, Frohlich KU, Schekman R. Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell 1995; 82: 885-893.
30. Rabouille C, Levine TP, Peters JM, Warren G. An NSF-like ATPase, p97, and NSF mediate cisternal regrowth from mitotic Golgi fragments. Cell 1995; 82: 905-914.
31. Hetzer M, Meyer HH, Walther TC, Bilbao-Cortes D, Warren G, Mattaj IW. Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat Cell Biol 2001; 3: 1086-1091.
32. Ye Y. Diverse functions with a common regulator: Ubiquitin takes command of an AAA ATPase. J Struct Biol 2006; 156: 29-40.
33. Schroer TA, Steuer ER, Sheetz MP. Cytoplasmic dynein is a minus end-directed motor for membranous organelles. Cell 1989; 56: 937-946.
34. Corthesy-Theulaz I, Pauloin A, Pfeffer SR. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J Cell Biol 1992; 118: 1333-1345.
35. Li YY, Yeh E, Hays T, Bloom K. Disruption of mitotic spindle orientation in a yeast dynein mutant. Proc Natl Acad Sci U S A 1993; 90: 10096-10100.
36. Goodenough U, Heuser J. Structural comparison of purified dynein proteins with in situ dynein arms. J Mol Biol 1984; 180: 1083-1118.
37. Gee MA, Heuser JE, Vallee RB. An extended microtubule-binding structure within the dynein motor domain. Nature 1997; 390: 636-639.
38. Koonce MP, Tikhonenko I. Functional elements within the dynein microtubule-binding domain. Mol Biol Cell 2000; 11: 523-529.
39. Habura A, Tikhonenko I, Chisholm RL, Koonce MP. Interaction mapping of a dynein heavy chain. Identification of dimerization and intermediate-chain binding domains. J Biol Chem 1999; 274: 15447-15453.
40. Tynan SH, Gee MA, Vallee RB. Distinct but overlapping sites within the cytoplasmic dynein heavy chain for dimerization and for intermediate chain and light intermediate chain binding. J Biol Chem 2000; 275: 32769-32774.
41. Oiwa K, Sakakibara H. Recent progress in dynein structure and mechanism. Curr Opin Cell Biol 2005; 17: 98-103.
42. Evans KJ, Gomes ER, Reisenweber SM, Gundersen GG, Lauring BP. Linking axonal degeneration to microtubule remodeling by Spastin-mediated microtubule severing. J Cell Biol 2005; 168: 599-606.
43. McNally FJ, Vale RD. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 1993; 75: 419-429.
44. Roll-Mecak A, Vale RD. The Drosophila homologue of the hereditary spastic paraplegia protein, spastin, severs and disassembles microtubules. Curr Biol 2005; 15: 650-655.
45. McNally K, Audhya A, Oegema K, McNally FJ. Katanin controls mitotic and meiotic spindle length. J Cell Biol 2006; 175: 881-891.
46. Hartman JJ, Mahr J, McNally K, Okawa K, Iwamatsu A, Thomas S, Cheesman S, Heuser J, Vale RD, McNally FJ. Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell 1998; 93: 277-287.
47. Zhang D, Rogers GC, Buster DW, Sharp DJ. Three microtubule severing enzymes contribute to the "Pacman-flux" machinery that moves chromosomes. J Cell Biol 2007; 177: 231-242.
48. Ahmad FJ, Yu W, McNally FJ, Baas PW. An essential role for katanin in severing microtubules in the neuron. J Cell Biol 1999; 145: 305-315.
49. Song HK, Hartmann C, Ramachandran R, Bochtler M, Behrendt R, Moroder L, Huber R. Mutational studies on HslU and its docking mode with HslV. Proc Natl Acad Sci U S A 2000; 97: 14103-14108.
50. Hinnerwisch J, Fenton WA, Furtak KJ, Farr GW, Horwich AL. Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 2005; 121: 1029-1041.
51. Mancini EJ, Kainov DE, Grimes JM, Tuma R, Bamford DH, Stuart DI. Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 2004; 118: 743-755.
52. White SR, Evans KJ, Lary J, Cole JL, Lauring B. Recognition of C-terminal amino acids in tubulin by pore loops in Spastin is important for microtubule severing. J Cell Biol 2007; 176: 995-1005.
53. Scott A, Chung HY, Gonciarz-Swiatek M, Hill GC, Whitby FG, Gaspar J, Holton JM, Viswanathan R, Ghaffarian S, Hill CP, Sundquist WI. Structural and mechanistic studies of VPS4 proteins. EMBO J 2005; 24: 3658-3669.
54. Graef M, Langer T. Substrate specific consequences of central pore mutations in the i-AAA protease Yme1 on substrate engagement. J Struct Biol 2006; 156: 101-108.
55. Hersch GL, Burton RE, Bolon DN, Baker TA, Sauer RT. Asymmetric interactions of ATP with the AAA+ ClpX6 unfoldase: Allosteric control of a protein machine. Cell 2005; 121: 1017-1027.
56. Martin A, Baker TA, Sauer RT. Rebuilt AAA+ motors reveal operating principles for ATP-fuelled machines. Nature 2005; 437: 1115-1120.
57. Doyle SM, Shorter J, Zolkiewski M, Hoskins JR, Lindquist S, Wickner S. Asymmetric deceleration of ClpB or Hsp104 ATPase activity unleashes protein-remodeling activity. Nat Struct Mol Biol 2007; 14: 114-122.
58. Evans K, Keller C, Pavur K, Glasgow K, Conn B, Lauring B. Interaction of two hereditary spastic paraplegia gene products, spastin and atlastin, suggests a common pathway for axonal maintenance. Proc Natl Acad Sci U S A 2006; 103: 10666-10671.
59. Nickerson DP, West M, Odorizzi G. Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes. J Cell Biol 2006; 175: 715-720.
60. Holzbaur EL, Hammarback JA, Paschal BM, Kravit NG, Pfister KK, Vallee RB. Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. Nature 1991; 351: 579-583.
61. Smith DS, Niethammer M, Ayala R, Zhou Y, Gambello MJ, Wynshaw-Boris A, Tsai LH. Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nat Cell Biol 2000; 2: 767-775.
62. Faulkner NE, Dujardin DL, Tai CY, Vaughan KT, O'Connell CB, Wang Y, Vallee RB. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat Cell Biol 2000; 2: 784-791.
63. Collins CA, Vallee RB. Preparation of microtubules from rat liver and testis: Cytoplasmic dynein is a major microtubule associated protein. Cell Motil Cytoskeleton 1989; 14: 491-500.
64. Hirokawa N, Sato-Yoshitake R, Yoshida T, Kawashima T. Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J Cell Biol 1990; 111: 1027-1037.
65. Azmi I, Davies B, Dimaano C, Payne J, Eckert D, Babst M, Katzmann DJ. Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. J Cell Biol 2006; 172: 705-717.
66. Lottridge JM, Flannery AR, Vincelli JL, Stevens TH. Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body. Proc Natl Acad Sci U S A 2006; 103: 6202-6207.
67. Rumpf S, Jentsch S. Functional division of substrate processing cofactors of the ubiquitin-selective Cdc48 chaperone. Mol Cell 2006; 21: 261-269.
68. Haslberger T, Weibezahn J, Zahn R, Lee S, Tsai FT, Bukau B, Mogk A. M domains couple the ClpB threading motor with the DnaK chaperone activity. Mol Cell 2007; 25: 247-260.
69. Lee S, Choi JM, Tsai FT. Visualizing the ATPase cycle in a protein disaggregating machine: Structural basis for substrate binding by ClpB. Mol Cell 2007; 25: 261-271.
70. Olbrich H, Haffner K, Kispert A, Volkel A, Volz A, Sasmaz G, Reinhardt R, Hennig S, Lehrach H, Konietzko N, Zariwala M, Noone PG, Knowles M, Mitchison HM, Meeks M et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet 2002; 30: 143-144.
71. Portsteffen H, Beyer A, Becker E, Epplen C, Pawlak A, Kunau WH, Dodt G. Human PEX1 is mutated in complementation group 1 of the peroxisome biogenesis disorders. Nat Genet 1997; 17: 449-452.
72. Reuber BE, Germain-Lee E, Collins CS, Morrell JC, Ameritunga R, Moser HW, Valle D, Gould SJ. Mutations in PEX1 are the most common cause of peroxisome biogenesis disorders. Nat Genet 1997; 17: 445-448.
73. Fukuda S, Shimozawa N, Suzuki Y, Zhang Z, Tomatsu S, Tsukamoto T, Hashiguchi N, Osumi T, Masuno M, Imaizumi K, Kuroki Y, Fujiki Y, Orii T, Kondo N. Human peroxisome assembly factor-2 (PAF-2): A gene responsible for group C peroxisome biogenesis disorder in humans. Am J Hum Genet 1996; 59: 1210-1220.
74. Yahraus T, Braverman N, Dodt G, Kalish JE, Morrell JC, Moser HW, Valle D, Gould SJ. The peroxisome biogenesis disorder group 4 gene, PXAAA1, encodes a cytoplasmic ATPase required for stability of the PTS1 receptor. EBMO J 1996; 15: 2914-2923.
75. Hinson JT, Fantin VR, Schonberger J, Breivik N, Siem G, McDonough B, Sharma P, Keogh I, Godinho R, Santos F, Esparza A, Nicolau Y, Selvaag E, Cohen BH, Hoppel CL et al. Missense mutations in the BCS1L gene as a cause of the Bjornstad syndrome. N Engl J Med 2007; 356: 809-819.
76. Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, Shalish C, de Leon D, Brin MF, Raymond D, Corey DP, Fahn S, Risch NJ, Buckler AJ, Gusella JF, Breakefield XO. The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet 1997; 17: 40-48.
77. Kustedjo K, Bracey MH, Cravatt BF. Torsin A and its torsion dystonia-associated mutant forms are lumenal glycoproteins that exhibit distinct subcellular localizations. J Biol Chem 2000; 275: 27933-27939.
78. Liu Z, Zolkiewska A, Zolkiewski M. Characterization of human torsinA and its dystonia-associated mutant form. Biochem J 2003; 374: 117-122.
79. Naismith TV, Heuser JE, Breakefield XO, Hanson PI. TorsinA in the nuclear envelope. Proc Natl Acad Sci U S A 2004; 101: 7612-7617.
80. Goodchild RE, Dauer WT. Mislocalization to the nuclear envelope: An effect of the dystonia-causing torsinA mutation. Proc Natl Acad Sci U S A 2004; 101: 847-852.
81. Goodchild RE, Dauer WT. The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J Cell Biol 2005; 168: 855-862.
82. Hazan J, Fonknechten N, Mavel D, Paternotte C, Samson D, Artiguenave F, Davoine CS, Cruaud C, Durr A, Wincker P, Brottier P, Cattolico L, Barbe V, Burgunder JM, Prud'homme JF et al. Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nat Genet 1999; 23: 296-303.
83. Baas PW, Joshi HC. Gamma-tubulin distribution in the neuron: implications for the origins of neuritic microtubules. J Cell Biol 1992; 119: 171-178.
84. Rugarli EI, Langer T. Translating m-AAA protease function in mitochondria to hereditary spastic paraplegia. Trends Mol Med 2006; 12: 262-269.
85. Nolden M, Ehses S, Koppen M, Bernacchia A, Rugarli EI, Langer T. The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Cell 2005; 123: 277-289.
86. Watts GD, Wymer J, Kovach MJ, Mehta SG, Mumm S, Darvish D, Pestronk A, Whyte MP, Kimonis VE. Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat Genet 2004; 36: 377-381.
87. Weihl CC, Dalal S, Pestronk A, Hanson PI. Inclusion body myopathy-associated mutations in p97/VCP impair endoplasmic reticulum-associated degradation. Hum Mol Genet 2006; 15: 189-199.
88. de Lonlay P, Valnot I, Barrientos A, Gorbatyuk M, Tzagoloff A, Taanman JW, Benayoun E, Chretien D, Kadhom N, Lombes A, de Baulny HO, Niaudet P, Munnich A, Rustin P, Rotig A. A mutant mitochondrial respiratory chain assembly protein causes complex III deficiency in patients with tubulopathy, encephalopathy and liver failure. Nat Genet 2001; 29: 57-60.
89. Visapaa I, Fellman V, Vesa J, Dasvarma A, Hutton JL, Kumar V, Payne GS, Makarow M, Van Coster R, Taylor RW, Turnbull DM, Suomalainen A, Peltonen L. GRACILE syndrome, a lethal metabolic disorder with iron overload, is caused by a point mutation in BCS1L. Am J Hum Genet 2002; 71: 863-876.