PEX12 interacts with PEX5 and PEX10 and acts downstream of receptor docking in peroxisomal matrix protein import

Journal of Cell Biology

Volumn 147, Issue 4, 1999, Pages 761-773

  Chang, Chia Che ^a   Warren, Daniel S ^a   Sacksteder, Katherine A ^a   Gould, Stephen J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Peroxisome biogenesis disorder; PEX10; PEX5; PTS1 receptor; Zellweger syndrome

Indexed keywords

BINDING PROTEIN; MEMBRANE PROTEIN;

ARTICLE; BIOGENESIS; GENE MUTATION; IMMUNOPRECIPITATION; MISSENSE MUTATION; PEROXISOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RECEPTOR BINDING; ZELLWEGER SYNDROME;

ALLELES; AMINO ACID SEQUENCE; BASE SEQUENCE; CELL LINE; DNA; DNA PRIMERS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; OPEN READING FRAMES; PEROXISOMAL DISORDERS; PEROXISOMES; POINT MUTATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; REPETITIVE SEQUENCES, NUCLEIC ACID; SKIN; TRANSFECTION; ZELLWEGER SYNDROME;

EID: 0033571690     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.4.761     Document Type: Article

References (74)

1. Adams, A., D.E. Gottschling, CA. Kaiser, and T. Stearns. 1997. Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press. Cold Spring Harbor. 115-116.
2. Albertini, M., P. Rehling, R. Erdmann, W. Girzalsky, J.A. Kiel, M. Veenhuis, and W.-H. Kunau. 1997. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell. 89:83-92.
3. Baes, M., P. Gressens, E. Baumgart, P. Carmeliet, M. Casteels, M. Fransen, P. Evrard, D. Fahimi, P.E. Declercq, D. Collen, P.P. van Veldhoven, and G.P. Mannaerts. 1997. A mouse model for Zellweger syndrome. Nat. Genet. 17: 49-57.
4. Borden, K.L. 1998. RING fingers and B-boxes: zinc-binding protein-protein interaction domains. Biochem. Cell Biol. 76:351-358.
5. Braverman, N., G. Dodt, S.J. Gould, and D. Valle. 1995. Disorders of peroxisome biogenesis. Hum. Mol. Genet. 4:1791-1798.
6. Braverman, N., G. Steel, C. Obie, A. Moser, H. Moser, S.J. Gould, and D. Valle. 1997. Human PEX7 encodes the peroxisomal PTS2 receptor and is responsible for rhizomelic chondrodysplasia punctata. Nat. Genet. 15:369-376.
7. Braverman, N., G. Dodt, S,J. Gould, and D. Valle. 1998. An isoform of Pex5p, the human PTS1 receptor, is required for the import of PTS2 proteins into peroxisomes. Hum. Mol. Genet. 7:1195-1205.
8. Chang, C.-C., and S.J. Gould. 1998. Phenotype-genotype relationships in complementation group 3 of the peroxisome-biogenesis disorders. Am. J. Hum. Genet. 63:1294-1306.
9. Chang, C.-C., W.-H. Lee, H.W. Moser, D. Valle, and S.J. Gould. 1997. Isolation of the human PEX12 gene, mutated in group 3 of the peroxisome biogenesis disorders. Nat. Genet. 15:385-388.
10. Chang, C.-C., S. South, D. Warren, J. Jones, A.B. Moser, H.W. Moser, and S.J. Gould. 1999. Metabolic control of peroxisome abundance. J. Cell Sci. 112: 1579-1590.
11. Chevray, P.M., and D. Nathans. 1992. Protein interaction cloning in yeast: identification of mammalian protein that reacts with the leucine zipper of Jun. Proc. Natl. Acad. Sci. USA. 89:5789-5793.
12. Collins, C.S., and S.J. Gould. 1999. Identification of a common mutation in severely affected PEXI -deficient patients. Hum. Mutat. 14:45-53.
13. Distel, B., R. Erdmann, S.J. Gould, G. Blobel, D.I. Crane, J.M. Cregg, G. Dodt, Y. Fujiki, J.M. Goodman, W.W. Just, et al. 1996. A unified nomenclature for peroxisome biogenesis. J. Cell Biol. 135:1-3.
14. Dodt, G., and S.J. Gould. 1996. Multiple PEX genes are required for proper subcellular distribution and stability of Pex5p, the PTS1 receptor: evidence that PTS1 protein import is mediated by a cycling receptor. J. Cell Biol. 135: 1763-1774.
15. Dodt, G., N. Braverman, C. Wong, A. Moser, H.W. Moser, P. Watkins, D. Valle, and S.J. Gould. 1995. Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat. Genet. 9:115-124.
16. Dyer, J.M., J. A. McNew, and J.M. Goodman. 1996. The sorting sequence of the peroxisomal integral membrane protein PMP47 is contained within a short hydrophilic loop. J. Cell Biol. 133:269-280.
17. Elgersma, Y., L. Kwast, A. Klein, T. Voom-Brouwer, M. van den Berg, B. Metzig, T. America, H.F. Tabak, and B. Distel. 1996. The SH3 domain of the Saccharomyces cerevisiae peroxisomal membrane protein Pex13p functions as a docking site for Pex5p, a mobile receptor for the import of PTS1-containing proteins. J. Cell Biol. 135:97-109.
18. Erdmann, R., and G. Blobel. 1996. Identification of Pex13p, a peroxisomal membrane receptor for the PTS1 recognition factor. J. Cell Biol. 135:111-121.
19. Erdmann, R., F.F. Wiebel, A. Flessau, J. Rytka, A. Beyer, K.U. Frohlich, and W.-H. Kunau. 1991. PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell. 64:499-510.
20. Evan, G.E., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
21. Faber, K.N., J.A. Heyman, and S. Subramani. 1998. Two AAA family proteins, PpPex1p and PpPex6p, interact with each other in an ATP-dependent manner and are associated with different subcellular membranous structures distinct from peroxisomes. Mol. Cell. Biol. 18:936-943.
22. Fransen, M., C. Brees, E. Baumgart, J.C.T. Vanhooren, M. Baes, G.P. Mannaerts, and P.P. van Veldhoven. 1995. Identification and characterization of the putative human peroxisomal terminal targeting signal import receptor. J. Biol. Chem. 270:7731-7736.
23. Fransen, M., S.R. Terlecky, and S. Subramani. 1998. Identification of a human PTS1 receptor docking protein directly required for peroxisomal protein import. Proc. Natl. Acad. Sci. USA. 95:8087-8092.
24. Fukuda, S., N. Shimozawa, Y. Suzuki, Z. Zhang, S. Tomatsu, T. Tsukamoto, N. Hashiguchi, T. Osumi, M. Masuno, K. Imaizumi, et al. 1996. Human peroxisome assembly factor-2 (PAF-2): a gene responsible for group C peroxisome biogenesis disorder in humans. Am. J. Hum. Genet. 59:1210-1220.
25. Geisbrecht, B.V., C.S. Collins, B.E. Reuber, and S.J. Gould. 1998. Disruption of a PEX1-PEX6 interaction is the most common cause of the neurologic disorders Zellweger syndrome, neonatal adrenoleukodystrophy, and infantile Refsum disease. Proc. Natl. Acad. Sci. USA. 95:8630-8635.
26. Girzalsky, W., P. Rehling, K. Stein, J. Kipper, L. Blank, W.H. Kunau, and R. Erdmann. 1999. Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J. Cell Biol. 144:1151-1162.
27. Gould, S.J., G.A. Keller, N. Hosken, J. Wilkinson, and S. Subramani. 1989. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108:1657-1664.
28. Gould, S.J., S. Krisans, G.A. Keller, and S. Subramani. 1990. Antibodies directed against the peroxisomal targeting signal of firefly luciferase recognize multiple mammalian peroxisomal proteins. J. Cell Biol. 110:27-34.
29. Gould, S.J., J.E. Kalish, J.C. Morrell, J. Bjorkman, A.J. Urquhart, and D.I. Crane. 1996. An SH3 protein in the peroxisome membrane is a docking factor for the PTS1 receptor. J. Cell Biol. 135:85-95.
30. Grant, S.G., J. Jessee, F.R. Bloom, and D. Hanahan. 1990. Differential plasmid rescue from ttansgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl. Acad. Sci. USA. 87:4645-4649.
31. Heyman, J.A., E. Mononsov, and S. Subramani. 1994. Role of the PAS1 gene of Pichia postoris in peroxisome biogenesis. J. Cell Biol. 127:1259-1273.
32. Honsho, M., S. Tamura, N. Shimozawa, Y. Suzuki, N. Kondo, and Y. Fujiki. 1998. Mutation in PEX16 is causal in the peroxisome-deficient Zellweger syndrome of complementation group D. Am. J. Hum. Genet. 63:1622-1630.
33. Huhse, B., P. Rehling, M. Albertini, L. Blank, K. Meller, and W.H. Kunau. 1998. Pex17p of Saccharomyces cerevisiae is a novel peroxin and component of the peroxisomal protein translocation machinery. J. Cell Biol. 140:49-60.
34. Kalish, J.E., C. Theda, J.C. Morrell, J.M. Berg, and S.J. Gould. 1995. Formation of the peroxisome lumen is abolished by loss of Pichia postoris Pas7p, a zinc-binding integral membrane protein of the peroxisome. Mol. Cell. Biol. 15: 6405-6419.
35. Kalish, J.E., G.A. Keller, J.C. Morrell, S.J. Mihalik, B. Smith, J.M. Cregg, and S.J. Gould. 1996. Characterization of a novel component of the peroxisomal protein import apparatus using fluorescent peroxisomal proteins. EMBO (Eur. Mol. Biol. Organ.) J. 15:3275-3285.
36. Lazarow, P.B., and Y. Fujiki. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1:489-530.
37. Lazarow, P.B., and H.W. Moser. 1995. Disorders of peroxisome biogenesis. In The Metabolic and Molecular Bases of Inherited Disease. C.R. Scriver, A.L. Beaudet, W.S. Sly, and D. Valle, editors. McGraw-Hill, New York. 2287-2324.
38. Liu, H., X. Tan, K.A. Russell, M. Veenhuis, and J.M. Cregg. 1995. PER3, a gene required for peroxisome biogenesis in Pichia postoris, encodes a peroxisomal membrane protein involved in protein import. J. Biol. Chem. 270: 10940-10951.
39. Liu, Y., J. Bjorkman, A. Urquhart, R.J.A. Wanders, D. Crane, and S.J. Gould. 1999. PEX13 is mutated in complementation group 13 of the peroxisome biogenesis disorders. Am. J. Hum. Genet. 65:621-634.
40. Marzioch, M., R. Erdmann, M. Veenhuis, and W.-H. Kunau. 1994. PAS7 encodes a novel yeast member of the WD-40 protein family essential for import of 3-oxoacyl-CoA thiolase, a PTS2-containing protein, into peroxisomes. EMBO (Eur. Mol. Biol. Organ.) J. 13:4908-4918.
41. Matlack, K.E., W. Mothes, and T.A. Rapoport. 1998. Protein translocation: tunnel vision. Cell. 92:381-390.
42. Matsuzono, Y., N. Kinoshita, S. Tamura, N. Shimozawa, M. Hamasaki, K. Ghaedi, R.J. Wanders, Y. Suzuki, N. Kondo, and Y. Fujiki. 1999. Human PEX19: cDNA cloning by functional complementation, mutation analysis in a patient with Zellweger syndrome, and potential role in peroxisomal membrane assembly. Proc. Nati Acad. Sci. USA. 96:2116-2121.
43. Mattaj, I.W., and L. Englmeier. 1998. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265-306.
44. McCollum, D., E. Monosov, and S. Subramani. 1993. The pas8 mutant of Pichia postoris exhibits the peroxisomal protein import deficiencies of Zellweger syndrome cells. The PAS8 protein binds to the COOH-terminal tripeptide peroxisomal targeting signal and is a member of the TPR protein family. J. Cell Biol. 121:761-774.
45. Motley, A.M., E.H. Hettema, E.M. Hogenhout, P. Brittes, A.L. ten Asbroek, F.A. Wijburg, F. Baas, H.S. Heijmans, H.F. Tabak, R.J.A. Wanders, and B. Distel. 1997. Rhizomelic chondrodysplasia punctata is a peroxisomal protein targeting disease caused by a non-functional PTS2 receptor. Nat. Genet. 15: 377-380.
46. Okumoto, K., and Y. Fujiki. 1997. PEX12 encodes an integral membrane protein of peroxisomes. Nat. Genet. 17:265-266.
47. Okumoto, K., R. Itoh, N. Shimozawa, Y. Suzuki, S. Tamura, N. Kondo, and Y. Fujiki. 1998a. Mutations in PEX10 is the cause of Zellweger peroxisome deficiency syndrome of complementation group B. Hum. Mol. Genet. 7:1399-1405.
48. Okumoto, K., N. Shimozawa, A. Kawai, S. Tamura, T. Tsukamoto, T. Osumi, H. Moser, R.J.A. Wanders, Y. Suzuki, N. Kondo, and Y. Fujiki. 1998b. PEX12, the pathogenic gene of group III Zellweger syndrome: cDNA cloning by functional complementation on a CHO cell mutant, patient analysis, and characterization of Pexl2p. Mol. Cell. Biol. 18:4324-4336.
49. Otera, H., K. Okumoto, K. Tateishi, Y. Ikoma, E. Matsuda, M. Mishimura, T. Tsukamoto, T. Osumi, K. Ohashi, O. Higuchi, and Y. Fujiki. 1998. Peroxisome targeting signal type-1 (PTS1) receptor is involved in import of both PTS1 and PTS2: studies with PEX5-defective CHO cell mutants. Mol. Cell. Biol. 18:388-399.
50. Pfanner, N., E.A. Craig, and A. Honlinger. 1997. Mitochondrial preprotein translocase. Annu. Rev. Cell Dev. Biol. 13:25-51.
51. Portsteffen, H., A. Beyer, E. Becker, C. Epplen, A. Pawlak, W.-H. Kunau, and G. Dodt. 1997. Human PEX1 is mutated in complementation group 1 of the peroxisome biogenesis disorders. Nat. Genet. 17:449-452.
52. Purdue, P.E., J.W. Zhang, M. Skoneczny, and P.B. Lazarow. 1997. Rhizomelic chondrodysplasia punctata is caused by deficiency of human PEX7 a homologue of the yeast PTS2 receptor. Nat. Genet. 15:381-384.
53. Rachubinski, R.A., and S. Subramani. 1995. How proteins penetrate peroxisomes. Cell. 83:525-528.
54. Reuber, B.E., E. Germain Lee, C.S. Collins, J.C. Morrell, R. Ameritunga, H.W. Moser, D. Valle, and S.J. Gould. 1997. Mutations in PEX1 are the most common cause of the peroxisome biogenesis disorders. Nat. Genet. 17:445-448.
55. Schatz, G., and B. Dobberstein. 1996. Common principles of protein translocation across membranes. Science. 271:1519-1526.
56. Schliebs, W., J. Saidowsky, B. Agianian, G. Dodt, F.W. Herberg, and W.H. Kunau. 1999. Recombinant human peroxisomal targeting signal receptor PEX5. Structural basis for interaction of PEX5 with PEX14. J. Biol. Chem. 274:5666-5673.
57. Shimozawa, N., T. Tsukamoto, Y. Suzuki, T. Orii, Y. Shirayoshi, T. Mori, and Y. Fujiki. 1992. A human gene responsible for Zellweger syndrome that affects peroxisome assembly. Science. 255:1132-1134.
58. Shimozawa, N., Y. Suzuki, Z. Zhang, A. Imamura, R. Toyama, S. Mukai, Y. Fujiki, T. Tsukamoto, T. Osumi, T. Orii, R.J.A. Wanders, and N. Kondo. 1999. Nonsense and temperature-sensitive mutations in PEX13 are the cause of complementation group H of peroxisome biogenesis disorders. Hum. Mol. Genet 8:1077-1083.
59. Slawecki, M., G. Dodt, S. Steinberg, A.B. Moser, H.W. Moser, and S.J. Gould. 1995. Identification of three distinct peroxisomal protein import defects in patients with peroxisomal biogenesis disorders. J. Cell Sci. 108:1817-1829.
60. South, S., and S.J. Gould. 1999. Peroxisome synthesis in the absence of preexisting peroxisomes. J. Cell Biol. 144:255-266.
61. Spong, A.P., and S. Subramani. 1993. Cloning and characterization of PAS5: a gene required for peroxisome biogenesis in the methylotrophic yeast Pichia pastoris.J. Cell Biol. 123:535-548.
62. Subramani, S. 1993. Protein import into peroxisomes and biogenesis of the organelle. Annu. Rev. Cell Biol. 9:445-178.
63. Swinkels, B.W., S.J. Gould, A.G. Bodnar, R.A. Rachubinski, and S. Subramani. 1991. A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO (Eur. Mol. Biol. Organ.) J. 10: 3244-3262.
64. Szilard, R.K., V.I. Titorenko, M. Veenhuis, and R.A. Rachubinski. 1995. Pay32p of the yeast Yarrowia lipolytica is an intraperoxisomal component of the matrix protein translocalion machinery. J. Cell Biol. 131:1453-1469.
65. Terlecky, S.R., W.M. Nuttley, D. McCollum, E. Sock, and S. Subramani. 1995. The Pichia postoris peroxisomal protein Pas8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO (Eur. Mol. Biol. Organ.) J. 14:3627-3634.
66. Titorenko, V.l., and R.A. Rachubinski. 1998a. The endoplasmic reticulum plays an essential role in peroxisome biogenesis. TIBS (Trends Biochem. Sci.). 23:231-233.
67. Titorenko, V.l., and R.A. Rachubinski. 1998b. Mutants of the yeast Yarrowia lipolytica defective in protein export exit from the endoplasmic reticulum are also defective in peroxisome biogenesis. Mol. Cell. Biol. 18:2789-2803.
68. Titorenko, V.I., D.M. Ogrydziak, and R.A. Rachubinski. 1997. Four distinct secretory pathways serve protein secretion, cell surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 17:5210-5226.
69. van der Klei, I.J., R.E. Hibrands, G.J. Swaving, H.R. Waterham, E.G. Vrieling, V.I. Titorenko, J.M. Cregg, W. Harder, and M. Veenhuis. 1995. The Hansenula polymorpha PER3 gene is essential for the import of PTS1 proteins into the peroxisome matrix. J. Biol. Chem. 270:17229-17236.
70. van der Klei, I.J., R.E. Hibrands, J.A. Kiel, S.W. Rasmussen, J.M. Cregg, and M. Veenhuis. 1998. The ubiquitin-conjugating enzyme Pex4p of Hansenula polymorpha is required for efficient functioning of the PTS1 import machinery. EMBO (Eur. Mol. Biol. Organ.) J. 17:3608-3618.
71. Vidal, M., R.K. Brachman, A. Fattaey, E. Harlow, and J.D. Boeke. 1996. Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc. Natl. Acad. Sci. USA. 93: 10315-10320.
72. Warren, D.S., J.C. Morrell, H.W. Moser, D. Valle, and S.J. Gould. 1998. Identification of PEX10, the gene defective in complementation group 7 of the peroxisome-biogenesis disorders. Am. J. Hum. Genet. 63:347-359.
73. Wiemer, E.A.C., W.M. Nuttley. B.L. Bertolaet, X. Li, U. Franke, M.J. Wheelock, W.K. Anne, K.R. Johnson, and S. Subramani. 1995. Human peroxisomal targeting signal-1 receptor restores peroxisomal protein import in cells from patients with fatal peroxisomal disorders. J. Cell Biol. 130:51-65.
74. Yahraus, T., N. Braverman, G. Dodt, J.E. Kalish, J.C. Morrell, H.W. Moser, D. Valle, and S.J. Gould. 1996. The peroxisome biogenesis disorder group 4 gene, PXAAA1, encodes a cytoplasmic ATPase required for stability of the PTS1 receptor. EMBO (Eur. Mol. Biol. Organ.) J. 15:2914-2923.