Molecular chaperone disorders: Defective Hsp60 in neurodegeneration

Current Topics in Medicinal Chemistry

Volumn 12, Issue 22, 2012, Pages 2491-2503

  Bross, Peter ^a   Magnoni, Raffaella ^a   Bie, Anne Sigaard ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

Chaperonin; Hsp60; Mitochondria; Motor neuron; Neurodegeneration; Protein quality control

Indexed keywords

CHAPERONIN 60; EARLY PREGNANCY FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOCHONDRIAL PROTEIN; POLYPEPTIDE; PROTEOLIPID PROTEIN;

AMINO ACID SEQUENCE; CELLULAR DISTRIBUTION; DEGENERATIVE DISEASE; DNA SEQUENCE; GENE EXPRESSION; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; LEUKODYSTROPHY; MITOCHONDRION; MYELINATION; NERVE DEGENERATION; NONHUMAN; PROTEIN FOLDING; REVIEW; SUDDEN INFANT DEATH SYNDROME;

ANIMALS; CHAPERONIN 10; CHAPERONIN 60; GENE EXPRESSION REGULATION; HUMANS; MAMMALS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR CHAPERONES; MUTATION; NEURODEGENERATIVE DISEASES; NEUROGLIA; PROTEIN FOLDING; SPASTIC PARAPLEGIA, HEREDITARY;

EID: 84874911348     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026611212220005     Document Type: Review

References (133)

1. Reading, D. S.; Hallberg, R. L.; Myers, A. M. Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor, Nature, 1989, 337(6208), 655-659.
2. McMullin, T. W. and Hallberg, R. L. A highly evolutionarily conserved mitochondrial protein is structurally related to the protein encoded by the Escherichia coli groEL gene, Mol. Cell Biol., 1988, 8(1), 371-380.
3. McMullin, T. W. and Hallberg, R. L. A normal mitochondrial protein is selectively synthesized and accumulated during heat shock in Tetrahymena thermophila, Mol. Cell Biol., 1987, 7(12), 4414-4423.
4. Georgopoulos, C. Toothpicks, Serendipity and the Emergence of the Escherichia coli DnaK (Hsp70) and GroEL (Hsp60) Chaperone Machines, Genetics, 2006, 174(4), 1699-1707.
5. Barraclough, R. and Ellis, R. J. Protein synthesis in chloroplasts. IX. Assembly of newly-synthesized large subunits into ribulose bisphosphate carboxylase in isolated intact pea chloroplasts, Biochim. Biophys. Acta, 1980, 608(1), 19-31.
6. Hemmingsen, S. M.; Woolford, C.; van der Vies, S. M.; Tilly, K.; Dennis, D. T.; Georgopoulos, C. P.; Hendrix, R. W.; Ellis, R. J. Homologous plant and bacterial proteins chaperone oligomeric protein assembly, Nature, 1988, 333(6171), 330-334.
7. Hemmingsen, S. M. What is a chaperonin? [letter], Nature, 1992, 357(6380), 650.
8. Kim, S.; Willison, K. R.; Horwich, A. L. Cystosolic chaperonin subunits have a conserved ATPase domain but diverged polypeptide-binding domains, Trends Biochem. Sci., 1994, 19(12), 543-548.
9. Tilly, K. and Georgopoulos, C. Evidence that the two Escherichia coli groE morphogenetic gene products interact in vivo, J. Bacteriol., 1982, 149(3), 1082-1088.
10. Lubben, T. H.; Gatenby, A. A.; Donaldson, G. K.; Lorimer, G. H.; Viitanen, P. V. Identification of a groES-like chaperonin in mitochondria that facilitates protein folding, Proc. Natl. Acad. Sci. U. S. A, 1990, 87(19), 7683-7687.
11. Hartman, D. J.; Hoogenraad, N. J.; Condron, R.; Hoj, P. B. Identification of a mammalian 10-kDa heat shock protein, a mitochondrial chaperonin 10 homologue essential for assisted folding of trimeric ornithine transcarbamoylase in vitro, Proc. Natl. Acad. Sci. U. S. A, 1992, 89(8), 3394-3398.
12. Hartman, D. J.; Dougan, D.; Hoogenraad, N. J.; Hoj, P. B. Heat shock proteins of barley mitochondria and chloroplasts. Identification of organellar hsp 10 and 12: putative chaperonin 10 homologues, FEBS Lett., 1992, 305(2), 147-150.
13. Ellis, R. J. and van der Vies, S. M. Molecular chaperones, Annu. Rev. Biochem., 1991, 60, 321-347.
14. Gething, M. J. and Sambrook, J. Protein folding in the cell, Nature, 1992, 355(6355), 33-45.
15. Cheng, M. Y.; Hartl, F. U.; Martin, J.; Pollock, R. A.; Kalousek, F.; Neupert, W.; Hallberg, E. M.; Hallberg, R. L.; Horwich, A. L. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria, Nature, 1989, 337(6208), 620-625.
16. Goloubinoff, P.; Gatenby, A. A.; Lorimer, G. H. GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli, Nature, 1989, 337(6202), 44-47.
17. Goloubinoff, P.; Christeller, J. T.; Gatenby, A. A.; Lorimer, G. H. Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfoleded state depends on two chaperonin proteins and Mg-ATP, Nature, 1989, 342(6252), 884-889.
18. Xu, Q.; Metzler, B.; Jahangiri, M.; Mandal, K. Molecular chaperones and heat shock proteins in atherosclerosis, Am. J. Physiol Heart Circ. Physiol, 2012, 302(3), H506-H514.
19. Henderson, B. and Pockley, A. G. Molecular chaperones and protein-folding catalysts as intercellular signaling regulators in immunity and inflammation, J. Leukoc. Biol., 2010, 88(3), 445-462.
20. Henderson, B. and Pockley, A. G. Proteotoxic stress and circulating cell stress proteins in the cardiovascular diseases, Cell Stress Chaperones., 2012, 17(3), 303-311.
21. Grundtman, C.; Kreutmayer, S. B.; Almanzar, G.; Wick, M. C.; Wick, G. Heat shock protein 60 and immune inflammatory responses in atherosclerosis, Arterioscler. Thromb. Vasc. Biol., 2011, 31(5), 960-968.
22. Ellis, R. J. and Hemmingsen, S. M. Molecular chaperones: proteins essential for the biogenesis of some macromolecular structures, Trends. Biochem. Sci., 1989, 14(8), 339-342.
23. Spiess, C.; Meyer, A. S.; Reissmann, S.; Frydman, J. Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets, Trends Cell Biol., 2004, 14(11), 598-604.
24. Kampinga, H. H.; Hageman, J.; Vos, M. J.; Kubota, H.; Tanguay, R. M.; Bruford, E. A.; Cheetham, M. E.; Chen, B.; Hightower, L. E. Guidelines for the nomenclature of the human heat shock proteins, Cell Stress. Chaperones., 2009, 14(1), 105-111.
25. Jindal, S.; Dudani, A. K.; Singh, B.; Harley, C. B.; Gupta, R. S. Primary structure of a human mitochondrial protein homologous to the bacterial and plant chaperonins and to the 65-kilodalton mycobacterial antigen, Mol. Cell Biol., 1989, 9(5), 2279-2283.
26. Picketts, D. J.; Mayanil, C. S.; Gupta, R. S. Molecular cloning of a Chinese hamster mitochondrial protein related to the chaperonin family of bacterial and plant proteins, J. Biol. Chem., 1989, 264(20), 12001-12008.
27. Venner, T. J.; Singh, B.; Gupta, R. S. Nucleotide sequences and novel structural features of human and Chinese hamster hsp60 (chaperonin) gene families, DNA Cell Biol., 1990, 9(8), 545-552.
28. Pochon, N. A. M. and Mach, B. Genetic complexity of the human hsp 60 gene, Int. Immunol., 1996, 8(2), 221-230.
29. Hansen, J. J.; Bross, P.; Westergaard, M.; Nielsen, M. N.; Eiberg, H.; Børglum, A. D.; Mogensen, J.; Kristiansen, K.; Bolund, L.; Gregersen, N. Genomic Structure of the Human Mitochondrial Chaperonin Genes: HSP60 and HSP10 are Localised Head to Head on Chromosome 2 Separated by a Bidirectional Promoter, Hum. Genet., 2003, 112(1), 71-77.
30. Ryan, M. T.; Herd, S. M.; Sberna, G.; Samuel, M. M.; Hoogenraad, N. J.; Hoj, P. B. The genes encoding mammalian chaperonin 60 and chaperonin 10 are linked head-to-head and share a bidirectional promoter, Gene, 1997, 196(1-2), 9-17.
31. Martin, C. C.; Tsang, C. H.; Beiko, R. G.; Krone, P. H. Expression and genomic organization of the zebrafish chaperonin gene complex, Genome, 2002, 45(5), 804-811.
32. Sarkar, S. and Lakhotia, S. C. The Hsp60C gene in the 25F cytogenetic region in Drosophila melanogaster is essential for tracheal development and fertility, J. Genet, 2005, 84(3), 265-281.
33. McQuilton, P.; St Pierre, S. E.; Thurmond, J. FlyBase 101-the basics of navigating FlyBase, Nucleic Acids Res., 2012, 40(Database issue), D706-D714.
34. Akerfelt, M.; Morimoto, R. I.; Sistonen, L. Heat shock factors: integrators of cell stress, development and lifespan, Nat Rev Mol Cell Biol, 2010, 11(8), 545-555.
35. Morton, J. P.; Kayani, A. C.; McArdle, A.; Drust, B. The exercise induced stress response of skeletal muscle, with specific emphasis on humans, Sports Med, 2009, 39(8), 643-662.
36. Zhao, Q.; Wang, J.; Levichkin, I. V.; Stasinopoulos, S.; Ryan, M. T.; Hoogenraad, N. J. A mitochondrial specific stress response in mammalian cells, EMBO J., 2002, 21(17), 4411-4419.
37. Broadley, S. A. and Hartl, F. U. Mitochondrial stress signaling: a pathway unfolds, Trends Cell Biol., 2008, 18(1), 1-4.
38. Wiseman, R. L.; Haynes, C. M.; Ron, D. SnapShot: The unfolded protein response, Cell, 2010, 140(4), 590.
39. Aldridge, J. E.; Horibe, T.; Hoogenraad, N. J. Discovery of Genes Activated by the Mitochondrial Unfolded Protein Response (mtUPR) and Cognate Promoter Elements, PLoS. ONE., 2007, 2(9), e874.
40. Horibe, T. and Hoogenraad, N. J. The chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response, PLoS. ONE., 2007, 2(9), e835.
41. Baker, B. M. and Haynes, C. M. Mitochondrial protein quality control during biogenesis and aging, Trends Biochem. Sci., 2011, 36(5), 254-261.
42. Haynes, C. M.; Yang, Y.; Blais, S. P.; Neubert, T. A.; Ron, D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans, Mol Cell, 2010, 37(4), 529-540.
43. Haynes, C. M. and Ron, D. The mitochondrial UPR - protecting organelle protein homeostasis, J. Cell Sci., 2010, 123(Pt 22), 3849-3855.
44. Kim, S. W. and Lee, J. K. NO-induced downregulation of HSP10 and HSP60 expression in the postischemic brain, J. Neurosci. Res., 2007, 85(6), 1252-1259.
45. Truettner, J. S.; Hu, K.; Liu, C. L.; Dietrich, W. D.; Hu, B. Subcellular stress response and induction of molecular chaperones and folding proteins after transient global ischemia in rats, Brain Res., 2009, 1249, 9-18.
46. Wang, Y.; Chen, L.; Hagiwara, N.; Knowlton, A. A. Regulation of heat shock protein 60 and 72 expression in the failing heart, J Mol Cell Cardiol., 2010, 48(2), 360-366.
47. Bonior, J.; Jaworek, J.; Konturek, S. J.; Pawlik, W. W. Leptin is the modulator of HSP60 gene expression in AR42J cells, J. Physiol Pharmacol., 2006, 57 Suppl 7, 135-143.
48. Kaufman, B. A.; Kolesar, J. E.; Perlman, P. S.; Butow, R. A. A function for the mitochondrial chaperonin Hsp60 in the structure and transmission of mitochondrial DNA nucleoids in Saccha romyces cerevisiae, J. Cell Biol., 2003, 163(3), 457-461.
49. Wang, Y. and Bogenhagen, D. F. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane, J. Biol. Chem., 2006, 281(35), 25791-25802.
50. Wong, P. and Houry, W. A. Chaperone networks in bacteria: analysis of protein homeostasis in minimal cells, J. Struct. Biol., 2004, 146(1-2), 79-89.
51. Brocchieri, L. and Karlin, S. Conservation among HSP60 sequences in relation to structure, function, and evolution, Protein Sci., 2000, 9(3), 476-486.
52. Karlin, S. and Brocchieri, L. Heat shock protein 60 sequence comparisons: duplications, lateral transfer, and mitochondrial evolution, Proc. Natl. Acad. Sci. U. S. A, 2000, 97(21), 11348-11353.
53. Hansen, J. J.; Dürr, A.; Cournu-Rebeix, I.; Georgopoulos, C.; Ang, D.; Nielsen, M. N.; Davoine, C. S.; Brice, A.; Fontaine, B.; Gregersen, N.; Bross, P. Hereditary Spastic Paraplegia SPG13 Is Associated with a Mutation in the Gene Encoding the Mitochondrial Chaperonin Hsp60, Am. J. Hum. Genet., 2002, 70(5), 1328-1332.
54. Bross, P.; Li, Z.; Hansen, J.; Hansen, J. J.; Nielsen, M. N.; Corydon, T. J.; Georgopoulos, C.; Ang, D.; Lundemose, J. B.; Niezen-Koning, K.; Eiberg, H.; Yang, H.; Kolvraa, S.; Bolund, L.; Gregersen, N. Single-nucleotide variations in the genes encoding the mitochondrial Hsp60/Hsp10 chaperone system and their disease-causing potential, J. Hum. Genet., 2007, 52(1), 56-65.
55. Hansen, J.; Svenstrup, K.; Ang, D.; Nielsen, M. N.; Christensen, J. H.; Gregersen, N.; Nielsen, J. E.; Georgopoulos, C.; Bross, P. A novel mutation in the HSPD1 gene in a patient with hereditary spastic paraplegia, J. Neurol., 2007, 254(7), 897-900.
56. Magen, D.; Georgopoulos, C.; Bross, P.; Ang, D.; Segev, Y.; Goldsher, D.; Nemirovski, A.; Shahar, E.; Ravid, S.; Luder, A.; Heno, B.; Gershoni-Baruch, R.; Skorecki, K.; Mandel, H. Mitochondrial hsp60 chaperonopathy causes an autosomalrecessive neurodegenerative disorder linked to brain hypomyelination and leukodystrophy, Am. J. Hum. Genet., 2008, 83(1), 30-42.
57. Itoh, H.; Kobayashi, R.; Wakui, H.; Komatsuda, A.; Ohtani, H.; Miura, A. B.; Otaka, M.; Masamune, O.; Andoh, H.; Koyama, K.; Sato, Y.; Tashima, Y. Mammalian 60-kDa stress protein (chaperonin homolog) - Identification, biochemical properties, and localization, J. Biol. Chem., 1995, 270, 13429-13435.
58. Kirchhoff, S. R.; Gupta, S.; Knowlton, A. A. Cytosolic heat shock protein 60, apoptosis, and myocardial injury, Circulation, 2002, 105(24), 2899-2904.
59. Chun, J. N.; Choi, B.; Lee, K. W.; Lee, D. J.; Kang, D. H.; Lee, J. Y.; Song, I. S.; Kim, H. I.; Lee, S. H.; Kim, H. S.; Lee, N. K.; Lee, S. Y.; Lee, K. J.; Kim, J.; Kang, S. W. Cytosolic Hsp60 is involved in the NF-kappaB-dependent survival of cancer cells via IKK regulation, PLoS. ONE., 2010, 5(3), e9422.
60. Hartl, F. U. and Hayer-Hartl, M. Converging concepts of protein folding in vitro and in vivo, Nat Struct. Mol Biol, 2009, 16(6), 574-581.
61. Nielsen, K. L.; McLennan, N.; Masters, M.; Cowan, N. J. A singlering mitochondrial chaperonin (Hsp60-Hsp10) can substitute for GroEL-GroES In vivo, J. Bacteriol., 1999, 181(18), 5871-5875.
62. Richardson, A.; Schwager, F.; Landry, S. J.; Georgopoulos, C. The importance of a mobile loop in regulating chaperonin/ cochaperonin interaction: humans versus Escherichia coli, J. Biol. Chem., 2001, 276(7), 4981-4987.
63. Horwich, A. L.; Fenton, W. A.; Chapman, E.; Farr, G. W. Two Families of Chaperonin: Physiology and Mechanism, Annu. Rev. Cell Dev. Biol., 2007, 23, 115-145.
64. Horwich, A. L. Protein folding in the cell: an inside story, Nat. Med., 2011, 17(10), 1211-1216.
65. Hartl, F. U. Chaperone-assisted protein folding: the path to discovery from a personal perspective, Nat. Med., 2011, 17(10), 1206-1210.
66. Brinker, A.; Pfeifer, G.; Kerner, M. J.; Naylor, D. J.; Hartl, F. U.; Hayer-Hartl, M. Dual Function of Protein Confinement in Chaperonin-Assisted Protein Folding, Cell, 2001, 107(2), 223-233.
67. Frank, G. A.; Goomanovsky, M.; Davidi, A.; Ziv, G.; Horovitz, A.; Haran, G. Out-of-equilibrium conformational cycling of GroEL under saturating ATP concentrations, Proc. Natl. Acad. Sci. U. S. A., 2010, 107(14), 6270-6274.
68. Lin, Z.; Madan, D.; Rye, H. S. GroEL stimulates protein folding through forced unfolding, Nat. Struct. Mol. Biol., 2008, 15(3), 303-311.
69. Ranson, N. A.; Farr, G. W.; Roseman, A. M.; Gowen, B.; Fenton, W. A.; Horwich, A. L.; Saibil, H. R. ATP-bound states of GroEL captured by cryo-electron microscopy, Cell, 2001, 107(7), 869-879.
70. Mayer, M. P. Gymnastics of molecular chaperones, Mol. Cell, 2010, 39(3), 321-331.
71. Lorimer, G. Protein folding - Folding with a two-stroke motor, Nature, 1997, 388(6644), 720.
72. Horwich, A. L.; Apetri, A. C.; Fenton, W. A. The GroEL/GroES cis cavity as a passive anti-aggregation device, FEBS Lett., 2009, 583(16), 2654-2662.
73. Sun, Z.; Scott, D. J.; Lund, P. A. Isolation and Characterisation of Mutants of GroEL that are Fully Functional as Single Rings, J. Mol. Biol., 2003, 332(3), 715-728.
74. Chatellier, J.; Hill, F.; Foster, N. W.; Goloubinoff, P.; Fersht, A. R. From Minichaperone to GroEL 3: Properties of an Active Singlering Mutant of GroEL, J. Mol. Biol., 2000, 304(5), 897-910.
75. Kovács, E.; Sun, Z.; Liu, H.; Scott, D. J.; Karsisiotis, A. I.; Clarke, A. R.; Burston, S. G.; Lund, P. A. Characterisation of a GroEL Single-Ring Mutant that Supports Growth of Escherichia coli and Has GroES-Dependent ATPase Activity, J. Mol. Biol., 2010, 396(5), 1271-1283.
76. Viitanen, P. V.; Lorimer, G. H.; Seetharam, R.; Gupta, R. S.; Oppenheim, J.; Thomas, J. O.; Cowan, N. J. Mammalian mitochon drial chaperonin 60 functions as a single toroidal ring, J. Biol. Chem., 1992, 267(2), 695-698.
77. Nielsen, K. L. and Cowan, N. J. A single ring is sufficient for productive chaperonin-mediated folding in vivo, Mol. Cell, 1998, 2(1), 93-99.
78. Levy-Rimler, G.; Viitanen, P.; Weiss, C.; Sharkia, R.; Greenberg, A.; Niv, A.; Lustig, A.; Delarea, Y.; Azem, A. The effect of nucleotides and mitochondrial chaperonin 10 on the structure and chaperone activity of mitochondrial chaperonin 60, Eur. J. Biochem., 2001, 268(12), 3465-3472.
79. Levy-Rimler, G.; Bell, R.; Ben Tal, N.; Azem, A. Type I chaperonins: not all are created equal, FEBS Lett., 2002, 529(1), 1.
80. Ellis, R. J. Roles of molecular chaperones in protein folding, Curr. Opin. Struct. Biol., 1994, 4(1), 117-122.
81. Jewett, A. I. and Shea, J. E. Reconciling theories of chaperonin accelerated folding with experimental evidence, Cell Mol. Life Sci., 2010, 67(2), 255-276.
82. Tang, Y. C.; Chang, H. C.; Chakraborty, K.; Hartl, F. U.; Hayer- Hartl, M. Essential role of the chaperonin folding compartment in vivo, EMBO J., 2008.
83. Hofmann, H.; Hillger, F.; Pfeil, S. H.; Hoffmann, A.; Streich, D.; Haenni, D.; Nettels, D.; Lipman, E. A.; Schuler, B. Singlemolecule spectroscopy of protein folding in a chaperonin cage, Proc. Natl. Acad. Sci. U. S. A., 2010, 107(26), 11793-11798.
84. Ewalt, K. L.; Hendrick, J. P.; Houry, W. A.; Hartl, F. U. In vivo observation of polypeptide flux through the bacterial chaperonin system, Cell, 1997, 90(3), 491-500.
85. Houry, W. A.; Frishman, D.; Eckerskorn, C.; Lottspeich, F.; Hartl, F. U. Identification of in vivo substrates of the chaperonin GroEL, Nature, 1999, 402(6758), 147-154.
86. Chaudhuri, T. K. and Gupta, P. Factors governing the substrate recognition by GroEL chaperone: a sequence correlation approach, Cell Stress. Chaperones., 2005, 10(1), 24-36.
87. Kerner, M. J.; Naylor, D. J.; Ishihama, Y.; Maier, T.; Chang, H. C.; Stines, A. P.; Georgopoulos, C.; Frishman, D.; Hayer-Hartl, M.; Mann, M.; Hartl, F. U. Proteome-wide analysis of chaperonin dependent protein folding in Escherichia coli, Cell, 2005, 122(2), 209-220.
88. Chapman, E.; Farr, G. W.; Usaite, R.; Furtak, K.; Fenton, W. A.; Chaudhuri, T. K.; Hondorp, E. R.; Matthews, R. G.; Wolf, S. G.; Yates, J. R.; Pypaert, M.; Horwich, A. L. Global aggregation of newly translated proteins in an Escherichia coli strain deficient of the chaperonin GroEL, Proc. Natl. Acad. Sci., 2006, 103(43), 15800-15805.
89. Fujiwara, K.; Ishihama, Y.; Nakahigashi, K.; Soga, T.; Taguchi, H. A systematic survey of in vivo obligate chaperonin-dependent substrates, EMBO J., 2010, 29(9), 1552-1564.
90. Raineri, E.; Ribeca, P.; Serrano, L.; Maier, T. A more precise characterization of chaperonin substrates, Bioinformatics, 2010, 26(14), 1685-1689.
91. Noivirt-Brik, O.; Unger, R.; Horovitz, A. Low folding propensity and high translation efficiency distinguish in vivo substrates of GroEL from other Escherichia coli proteins, Bioinformatics, 2007, 23(24), 3276-3279.
92. Dubaquie, Y.; Looser, R.; Fünfschilling, U.; Jenö, P.; Rospert, S. Identification of in vivo substrates of the yeast mitochondrial chaperonins reveals overlapping but non-identical requirement for hsp60 and hsp10, EMBO J., 1998, 17(20), 5868-5876.
93. Saijo, T.; Welch, W. J.; Tanaka, K. Intramitochondrial folding and assembly of medium-chain acyl-CoA dehydrogenase (MCAD) - Demonstration of impaired transfer of K304E-variant MCAD from its complex with Hsp60 to the native tetramer, J. Biol. Chem., 1994, 269, 4401-4408.
94. Corydon, T. J.; Hansen, J.; Bross, P.; Jensen, T. G. Downregulation of Hsp60 expression by RNAi impairs folding of medium-chain acyl-CoA dehydogenase wild-type and diseaseassociated proteins, Mol. Genet. Metab, 2005, 85(4), 260-270.
95. Bross, P.; Andresen, B. S.; Winter, V.; Kräutle, F.; Jensen, T. G.; Nandy, A.; Kølvraa, S.; Ghisla, S.; Bolund, L.; Gregersen, N. Cooverexpression of bacterial GroESL chaperonins partly overcomes non-productive folding and tetramer assembly of E.coli- expressed human medium-chain acyl-CoA dehydrogenase (MCAD) carrying the prevalent disease-causing K304E mutation, Biochim. Biophys. Acta, 1993, 1182, 264-274.
96. Bross, P.; Jespersen, C.; Jensen, T. G.; Andresen, B. S.; Kristensen, M. J.; Winter, V.; Nandy, A.; Kräutle, F.; Ghisla, S.; Bolund, L.; Kim, J. J. P.; Gregersen, N. Effects of two mutations detected in medium chain acyl-CoA dehydrogenase (MCAD)-deficient patients on folding, oligomer assembly, and stability of MCAD enzyme, J. Biol. Chem., 1995, 270, 10284-10290.
97. Jensen, T. G.; Bross, P.; Andresen, B. S.; Lund, T. B.; Kristensen, T. J.; Jensen, U. B.; Winther, V.; Kølvraa, S.; Gregersen, N.; Bolund, L. Comparison between medium-chain acyl-CoA dehydro genase mutant proteins overexpressed in bacterial and mammalian cells, Hum. Mutat., 1995, 6(3), 226-231.
98. Andresen, B. S.; Bross, P.; Udvari, S.; Kirk, J.; Gray, G.; Kmoch, S.; Chamoles, N.; Knudsen, I.; Winter, V.; Wilcken, B.; Yokota, I.; Hart, K.; Packman, S.; Harpey, J. P.; Saudubray, J. M.; Hale, D. E.; Bolund, L.; Kølvraa, S.; Gregersen, N. The molecular basis of medium-chain acyl-CoA dehydrogenase (MCAD) deficiency in compound heterozygous patients: Is there correlation between genotype and phenotype?, Hum. Mol. Genet., 1997, 6(5), 695-707.
99. Tokuriki, N. and Tawfik, D. S. Chaperonin overexpression promotes genetic variation and enzyme evolution, Nature, 2009, 459(7247), 668-673.
100. Williams, T. A.; Fares, M. A. The effect of chaperonin buffering on protein evolution, Genome Biol. Evol., 2010, 2, 609-619.
101. Fares, M. A.; Moya, A.; Barrio, E. GroEL and the maintenance of bacterial endosymbiosis, Trends Genet., 2004, 20(9), 413-416.
102. Fares, M. A.; Ruiz-Gonzalez, M. X.; Moya, A.; Elena, S. F.; Barrio, E. Endosymbiotic bacteria: GroEL buffers against deleterious mutations, Nature, 2002, 417(6887), 398.
103. Bie, A. S.; Palmfeldt, J.; Hansen, J.; Christensen, R.; Gregersen, N.; Corydon, T. J.; Bross, P. A cell model to study different degrees of Hsp60 deficiency in HEK293 cells, Cell Stress Chaperones., 2011, 16(6), 633-640.
104. Agsteribbe, E.; Huckriede, A.; Veenhuis, M.; Ruiters, M. H.; Niezen-Koning, K. E.; Skjeldal, O. H.; Skullerud, K.; Gupta, R. S.; Hallberg, R.; van Diggelen, O. P., et al., A fatal, systemic mito chondrial disease with decreased mitochondrial enzyme activities, abnormal ultrastructure of the mitochondria and deficiency of heat shock protein 60, Biochem. Biophys. Res. Commun., 1993, 193(1), 146-154.
105. Huckriede, A. and Agsteribbe, E. Decreased synthesis and inefficient mitochondrial import of hsp60 in a patient with a mitochondrial encephalomyopathy, Bba-Mol. Basis. Dis., 1994, 1227, 200-206.
106. Huckriede, A.; Heikema, A.; Sjollema, K.; Briones, P.; Agsteribbe, E. Morphology of the mitochondria in heat shock protein 60 deficient fibroblasts from mitochondrial myopathy patients. Effects of stress conditions, Virchows Archiv., 1995, 427(2), 159-165.
107. Briones, P.; Vilaseca, M. A.; Ribes, A.; Vernet, A.; Lluch, M.; Cusi, V.; Huckriede, A.; Agsteribbe, E. A new case of multiple mitochondrial enzyme deficiencies with decreased amount of heat shock protein 60, J. Inherited Metab. Dis., 1997, 20(4), 569-577.
108. Courts, C. and Madea, B. Genetics of the sudden infant death syndrome, Forensic Sci. Int., 2010, 203(1-3), 25-33.
109. Rahim, R. A.; Boyd, P. A.; Ainslie Patrick, W. J.; Burdon, R. H. Human heat shock protein gene polymorphisms and sudden infant death syndrome, Arch. Dis. Child, 1996, 75(5), 451-452.
110. Schon, E. A. and Przedborski, S. Mitochondria: the next (neurode) generation, Neuron, 2011, 70(6), 1033-1053.
111. McBride, H. M.; Neuspiel, M.; Wasiak, S. Mitochondria: more than just a powerhouse, Curr. Biol., 2006, 16(14), R551-R560.
112. Haas, R. H.; Parikh, S.; Falk, M. J.; Saneto, R. P.; Wolf, N. I.; Darin, N.; Cohen, B. H. Mitochondrial disease: a practical approach for primary care physicians, Pediatrics, 2007, 120(6), 1326-1333.
113. Kwong, J. Q.; Beal, M. F.; Manfredi, G. The role of mitochondria in inherited neurodegenerative diseases, J. Neurochem., 2006, 97(6), 1659-1675.
114. Mandemakers, W.; Morais, V. A.; De, S. B. A cell biological perspective on mitochondrial dysfunction in Parkinson disease and other neurodegenerative diseases, J. Cell Sci., 2007, 120(Pt 10), 1707-1716.
115. Petrozzi, L.; Ricci, G.; Giglioli, N. J.; Siciliano, G.; Mancuso, M. Mitochondria and neurodegeneration, Biosci. Rep., 2007, 27(1-3), 87-104.
116. Davison, E. J.; Pennington, K.; Hung, C. C.; Peng, J.; Rafiq, R.; Ostareck-Lederer, A.; Ostareck, D. H.; Ardley, H. C.; Banks, R. E.; Robinson, P. A. Proteomic analysis of increased Parkin expression and its interactants provides evidence for a role in modulation of mitochondrial function, Proteomics, 2009, 9(18), 4284-4297.
117. Rakovic, A.; Grunewald, A.; Voges, L.; Hofmann, S.; Orolicki, S.; Lohmann, K.; Klein, C. PINK1-Interacting Proteins: Proteomic Analysis of Overexpressed PINK1. Parkinson's Dis., 2011, 2011, 1539-1579.
118. Jin, J.; Li, G. J.; Davis, J.; Zhu, D.; Wang, Y.; Pan, C.; Zhang, J. Identification of Novel Proteins Associated with Both alpha- Synuclein and DJ-1, Mol. & Cell. Proteom., 2007, 6(5), 845-859.
119. DiMauro, S.; Schon, E. A. Mitochondrial disorders in the nervous system, Annu. Rev. Neurosci., 2008, 31, 91-123.
120. Rugarli, E. I. and Langer, T. Mitochondrial quality control: a matter of life and death for neurons, EMBO J., 2012, 31(6), 1336-1349.
121. Casari, G. and Marconi, R. Spastic Paraplegia 7. Pagon, R. A. Bird, D. T. Dolan, C. R. Stephens, K. and Adam, M. P. Gene Reviews TM [Internet]. 1993. Seattle, University of Washington.
122. Maltecca, F.; Magnoni, R.; Cerri, F.; Cox, G. A.; Quattrini, A.; Casari, G. Haploinsufficiency of AFG3L2, the gene responsible for spinocerebellar ataxia type 28, causes mitochondria-mediated Purkinje cell dark degeneration, J Neurosci, 2009, 29(29), 9244-9254.
123. Pierson, T. M.; Adams, D.; Bonn, F.; Martinelli, P.; Cherukuri, P. F.; Teer, J. K.; Hansen, N. F.; Cruz, P.; Mullikin For The Nisc Comparative Sequencing Program JC; Blakesley, R. W.; Golas, G.; Kwan, J.; Sandler, A.; Fuentes, F. K.; Markello, T.; Tifft, C.; Blackstone, C.; Rugarli, E. I.; Langer, T.; Gahl, W. A.; Toro, C. Whole-exome sequencing identifies homozygous AFG3L2 mutations in a spastic ataxia-neuropathy syndrome linked to mito chondrial m-AAA proteases, PLoS. Genet., 2011, 7(10), e1002325.
124. Blackstone, C.; O'Kane, C. J.; Reid, E. Hereditary spastic paraplegias: membrane traffic and the motor pathway, Nat. Rev. Neurosci., 2011, 12(1), 31-42.
125. Bross, P.; Naundrup, S.; Hansen, J.; Nielsen, M. N.; Christensen, J. H.; Kruhoffer, M.; Palmfeldt, J.; Corydon, T. J.; Gregersen, N.; Ang, D.; Georgopoulos, C.; Nielsen, K. L. The HSP60-(P.val98ile) mutation associated with hereditary spastic paraplegia SPG13 compromises chaperonin function both in vitro and in vivo, J. Biol. Chem., 2008, 283(23), 15694-15700.
126. Parnas, A.; Nadler, M.; Nisemblat, S.; Horovitz, A.; Mandel, H.; Azem, A. The MitCHAP-60 disease is due to entropic destabilization of the human mitochondrial Hsp60 oligomer, J Biol Chem, 2009, 284(41), 28198-28203.
127. Svenstrup, K.; Giraud, G.; Boespflug-Tanguy, O.; Danielsen, E. R.; Thomsen, C.; Rasmussen, K.; Law, I.; Vogel, A.; Stokholm, J.; Crone, C.; Hjermind, L. E.; Nielsen, J. E. Hereditary spastic paraplegia caused by the PLP1 'rumpshaker mutation', J. Neurol. Neurosurg. Psychiatry, 2010, 81(6), 666-672.
128. Fukumura, S.; Adachi, N.; Nagao, M.; Tsutsumi, H. A novel proteolipid protein 1 gene mutation causing classical type Pelizaeus-Merzbacher disease, Brain Dev., 2011, 33(8), 697-699.
129. Dick, K. J.; Eckhardt, M.; Paisan-Ruiz, C.; Alshehhi, A. A.; Proukakis, C.; Sibtain, N. A.; Maier, H.; Sharifi, R.; Patton, M. A.; Bashir, W.; Koul, R.; Raeburn, S.; Gieselmann, V.; Houlden, H.; Crosby, A. H. Mutation of FA2H underlies a complicated form of hereditary spastic paraplegia (SPG35), Hum. Mutat., 2010, 31(4), E1251-E1260.
130. Edvardson, S.; Hama, H.; Shaag, A.; Gomori, J. M.; Berger, I.; Soffer, D.; Korman, S. H.; Taustein, I.; Saada, A.; Elpeleg, O. Mutations in the fatty acid 2-hydroxylase gene are associated with leukodystrophy with spastic paraparesis and dystonia, Am. J. Hum. Genet., 2008, 83(5), 643-648.
131. Nave, K. A. Myelination and support of axonal integrity by glia, Nature, 2010, 468(7321), 244-252.
132. Perezgasga, L.; Segovia, L.; Zurita, M. Molecular characterization of the 5' control region and of two lethal alleles affecting the hsp60 gene in Drosophila melanogaster, FEBS Lett., 1999, 456(2), 269-273.
133. Christensen, J. H.; Nielsen, M. N.; Hansen, J.; Fuchtbauer, A.; Fuchtbauer, E. M.; West, M.; Corydon, T. J.; Gregersen, N.; Bross, P. Inactivation of the hereditary spastic paraplegia-associated Hspd1 gene encoding the Hsp60 chaperone results in early embryonic lethality in mice, Cell Stress. Chaperones., 2010, 15(6), 851-863.