Alternative splicing of human insulin-degrading enzyme yields a novel isoform with a decreased ability to degrade insulin and amyloid β-protein

Biochemistry

Volumn 44, Issue 17, 2005, Pages 6513-6525

  Farris, Wesley ^a   Leissring, Malcolm A ^a   Hemming, Matthew L ^a   Chang, Alice Y ^a   Selkoe, Dennis J ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HIM 730 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; DEGRADATION; DIMERS; DISEASES; FLUORESCENCE; GENETIC ENGINEERING; GLUCOSE; INSULIN; RNA;

ALZHEIMER'S DISEASE (AD); CEREBRAL AMYLOID; INSULIN-DEGRADING ENZYMES (IDE); PATHOLOGICAL MUTATIONS;

ENZYMES;

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; INSULIN; INSULINASE; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CATALYSIS; CELL FRACTIONATION; CELL ORGANELLE; CELLULAR DISTRIBUTION; CHO CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; EXON; GENE MUTATION; GENETIC TRANSCRIPTION; IMMUNOFLUORESCENCE; IMMUNOGOLD ELECTRON MICROSCOPY; INSULIN DEGRADATION; KINETICS; MITOCHONDRION; MOLECULAR WEIGHT; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN VARIANT;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN; ANIMALS; BASE SEQUENCE; CATALYTIC DOMAIN; CHO CELLS; CRICETINAE; CYTOSOL; DIMERIZATION; EXONS; HUMANS; INSULIN; INSULYSIN; ISOENZYMES; KINETICS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; RNA 3' POLYADENYLATION SIGNALS; RNA, MESSENGER; SUBSTRATE SPECIFICITY; TRANSCRIPTION INITIATION SITE;

LEUCISCUS IDUS;

EID: 17844382678     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0476578     Document Type: Article

References (53)

1. Duckworth, W. C., Bennett, R. G., and Hamel, F. G. (1998) Insulin degradation: Progress and potential, Endocr. Rev. 19, 608-624.
2. Leissring, M. A., Farris, W., Wu, X., Christodoulou, D. C., Haigis, M. C., Guarente, L., and Selkoe, D. J. (2004) Alternative translation initiation generates a novel isoform of insulin-degrading enzyme targeted to mitochondria, Biochem. J. 383, 439-446.
3. Edbauer, D., Willem, M., Lammich, S., Steiner, H., and Haass, C. (2002) Insulin-degrading enzyme rapidly removes the β-amyloid precursor protein intracellular domain (AICD), J. Biol. Chem. 277, 13389-13393.
4. Bennett, R. G., Duckworth, W. C., and Hamel, F. G. (2000) Degradation of amylin by insulin-degrading enzyme, J. Biol. Chem. 275, 36621-36625.
5. Farris, W., Mansourian, S., Chang, Y., Lindsley, L., Eckman, E. A., Frosch, M. P., Eckman, C. B., Tanzi, R. E., Selkoe, D. J., and Guenette, S. (2003) Insulin-degrading enzyme regulates the levels of insulin, amyloid β-protein, and the β-amyloid precursor protein intracellular domain in vivo, Proc. Natl. Acad. Sci. U.S.A. 100, 4162-4167.
6. Miller, B. C., Eckman, E. A., Sambamurti, K., Dobbs, N., Chow, K. M., Eckman, C. B., Hersh, L. B., and Thiele, D. L. (2003) Amyloid-β peptide levels in brain are inversely correlated with insulysin activity levels in vivo, Proc. Natl. Acad. Sci. U.S.A. 100, 6221-6226.
7. Farris, W., Mansourian, S., Leissring, M. A., Eckman, E. A., Bertram, L., Eckman, C. B., Tanzi, R. E., and Selkoe, D. J. (2004) Partial loss-of-function mutations in insulin-degrading enzyme that induce diabetes also impair degradation of amyloid β-protein, Am. J. Pathol. 164, 1425-1434.
8. Bertram, L., Blacker, D., Mullin, K., Keeney, D., Jones, J., Basu, S., Yhu, S., Mclnnis, M. G., Go, R. C., Vekrellis, K., Selkoe, D. J., Saunders, A. J., and Tanzi, R. E. (2000) Evidence for genetic linkage of Alzheimer's disease to chromosome 10q, Science 290, 2302-2303.
9. Ghosh, S., Watanabe, R. M., Valle, T. T., Hauser, E. R., Magnuson, V. L., Langefeld, C. D., Ally, D. S., Mohlke, K. L., Silander, K., Kohtamaki, K., Chines, P., Balow, J., Jr., Birznieks, G., Chang, J., Eldridge, W., Erdos, M. R., Karanjawala, Z. E., Knapp, J. I., Kudelko, K., Martin, C., Morales-Mena, A., Musick, A., Musick, T., Pfahl, C., Porter, R., and Rayman, J. B. (2000) The Finland-United States investigation of non-insulin-dependent diabetes mellitus genetics (FUSION) study. I. An autosomal genome scan for genes that predispose to type 2 diabetes, Am. J. Hum. Genet. 67, 1174-1185.
10. Wiltshire, S., Hattersley, A. T., Hitman, G. A., Walker, M., Levy, J. C., Sampson, M., O'Rahilly, S., Frayling, T. M., Bell, J. I., Lathrop, G. M., Bennett, A., Dhillon, R., Fletcher, C., Groves, C. J., Jones, E., Prestwich, P., Simecek, N., Rao, P. V., Wishart, M., Bottazzo, G. F., Foxon, R., Howell, S., Smedley, D., Cardon, L. R., Menzel, S., and McCarthy, M. I. (2001) A genomewide scan for loci predisposing to type 2 diabetes in a U.K. population (the Diabetes UK Warren 2 Repository): Analysis of 573 pedigrees provides independent replication of a susceptibility locus on chromosome 1q, Am. J. Hum. Genet. 69, 553-569.
11. Meigs, J. B., Panhuysen, C. I., Myers, R. H., Wilson, P. W., and Cupples, L. A. (2002) A genome-wide scan for loci linked to plasma levels of glucose and HbA(lc) in a community-based sample of Caucasian pedigrees: The Framingham Offspring Study, Diabetes 51, 833-840.
12. Ait-Ghezala, G., Abdullah, L., Crescentini, R., Crawford, F., Town, T., Singh, S., Richards, D., Duara, R., and Mullan, M. (2002) Confirmation of association between D10S583 and Alzheimer's disease in a case-control sample, Neurosci. Lett. 325, 87-90.
13. Edland, S. D., Wavrant-De Vriese, F., Compton, D., Smith, G. E., Ivnik, R., Boeve, B. F., Tangalos, E. G., and Petersen, R. C. (2003) Insulin degrading enzyme (IDE) genetic variants and risk of Alzheimer's disease: Evidence of effect modification by apolipoprotein E (APOE), Neurosci. Lett. 345, 21-24.
14. Prince, J. A., Feuk, L., Gu, H. F., Johansson, B., Gatz, M., Blennow, K., and Brookes, A. J. (2003) Genetic variation in a haplotype block spanning IDE influences Alzheimer disease, Hum. Mutat. 22, 363-371.
15. Bian, L., Yang, J. D., Guo, T. W., Sun, Y., Duan, S. W., Chen, W. Y., Pan, Y. X., Feng, G. Y., and He, L. (2004) Insulin-degrading enzyme and Alzheimer disease: A genetic association study in the Han Chinese, Neurology 63, 241-245.
16. Ertekin-Taner, N., Allen, M., Fadale, D., Scanlin, L., Younkin, L., Petersen, R. C., Graff-Radford, N., and Younkin, S. G. (2004) Genetic variants in a haplotype block spanning IDE are significantly associated with plasma Aβ42 levels and risk for Alzheimer disease, Hum. Mutat. 23, 334-342.
17. Karamohamed, S., Demissie, S., Volcjak, J., Liu, C., Heard-Costa, N., Liu, J., Shoemaker, C. M., Panhuysen, C. I., Meigs, J. B., Wilson, P., Atwood, L. D., Cupples, L. A., and Herbert, A. (2003) Polymorphisms in the Insulin-Degrading Enzyme Gene Are Associated With Type 2 Diabetes in Men From the NHLBI Framingham Heart Study, Diabetes 52, 1562-1567.
18. Gu, H. F., Efendic, S., Nordman, S., Ostenson, C. G., Brismar, K., Brookes, A. J., and Prince, J. A. (2004) Quantitative trait loci near the insulin-degrading enzyme (IDE) gene contribute to variation in plasma insulin levels, Diabetes 53, 2137-2142.
19. Abraham, R., Myers, A., Wavrant-DeVrieze, F., Hamshere, M. L., Thomas, H. V., Marshall, H., Compton, D., Spurlock, G., Turic, D., Hoogendoorn, B., Kwon, J. M., Petersen, R. C., Tangalos, E., Norton, J., Morris, J. C., Bullock, R., Liolitsa, D., Lovestone, S., Hardy, J., Goate, A., O'Donovan, M., Williams, J., Owen, M. J., and Jones, L. (2001) Substantial linkage disequilibrium across the insulin-degrading enzyme locus but no association with late-onset Alzheimer's disease, Hum. Genet. 109, 646-652.
20. Boussaha, M., Hannequin, D., Verpillat, P., Brice, A., Frebourg, T., and Campion, D. (2002) Polymorphisms of insulin degrading enzyme gene are not associated with Alzheimer's disease, Neurosci. Lett. 329, 121-123.
21. Sakai, A., Ujike, H., Nakata, K., Takehisa, Y., Imamura, T., Uchida, N., Kanzaki, A., Yamamoto, M., Fujisawa, Y., Okumura, K., and Kuroda, S. (2004) No association between the insulin degrading enzyme gene and Alzheimer's disease in a Japanese population, Am. J. Med. Genet. 125B, 87-91.
22. Groves, C. J., Wiltshire, S., Smedley, D., Owen, K. R., Frayling, T. M., Walker, M., Hitman, G. A., Levy, J. C., O'Rahilly, S., Menzel, S., Hattersley, A. T., and McCarthy, M. I. (2003) Association and haplotype analysis of the insulin-degrading enzyme (IDE) gene, a strong positional and biological candidate for type 2 diabetes susceptibility, Diabetes 52, 1300-1305.
23. Leibson, C. L., Rocca, W. A., Hanson, V. A., Cha, R., Kokmen, E., O'Brien, P. C., and Palumbo, P. J. (1997) Risk of dementia among persons with diabetes mellitus: A population-based cohort study, Am. J. Epidemiol. 145, 301-308.
24. Ott, A., Stolk, R. P., van Harskamp, F., Pols, H. A., Hofman, A., and Breteler, M. M. (1999) Diabetes mellitus and the risk of dementia: The Rotterdam Study, Neurology 53, 1937-1942.
25. Luchsinger, J. A., Tang, M. X., Stern, Y., Shea, S., and Mayeux, R. (2001) Diabetes mellitus and risk of Alzheimer's disease and dementia with stroke in a multiethnic cohort, Am. J. Epidemiol. 154, 635-641.
26. Peila, R., Rodriguez, B. L., and Launer, L. J. (2002) Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: The Honolulu-Asia Aging Study, Diabetes 51, 1256-1262.
27. Razay, G., and Wilcock, G. K. (1994) Hyperinsulinaemia and Alzheimer's disease, Age Ageing 23, 396-399.
28. Kuusisto, J., Koivisto, K., Mykkanen, L., Helkala, E. L., Vanhanen, M., Hanninen, T., Kervinen, K., Kesaniemi, Y. A., Riekkinen, P. J., and Laakso, M. (1997) Association between features of the insulin resistance syndrome and Alzheimer's disease independently of apolipoprotein E4 phenotype: Cross sectional population based study, BMJ [Br. Med. J.] 315, 1045-1049.
29. Arvanitakis, Z., Wilson, R. S., Bienias, J. L., Evans, D. A., and Bennett, D. A. (2004) Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch. Neurol. 61, 661-666.
30. Kuo, W. L., Gehm, B. D., and Rosner, M. R. (1990) Cloning and expression of the cDNA for a Drosophila insulin-degrading enzyme, Mol. Endocrinol. 4, 1580-1591.
31. Baumeister, H., Muller, D., Rehbein, M., and Richter, D. (1993) The rat insulin-degrading enzyme. Molecular cloning and characterization of tissue-specific transcripts. FEBS Lett. 317, 250-254.
32. Kuo, W. L., Montag, A. G., and Rosner, M. R. (1993) Insulin-degrading enzyme is differentially expressed and developmentally regulated in various rat tissues, Endocrinology 132, 604-611.
33. Affholter, J. A., Fried, V. A., and Roth, R. A. (1988) Human insulin-degrading enzyme shares structural and functional homologies with E. coli protease III, Science 242, 1415-1418.
34. Ota, T., Suzuki, Y., Nishikawa, T., Otsuki, T., Sugiyama, T., Irie, R., Wakamatsu, A., Hayashi, K., Sato, H., Nagai, K., Kimura, K., Makita, H., Sekine, M., Obayashi, M., Nishi, T., Shibahara, T., Tanaka, T., Ishii, S., Yamamoto, J., Saito, K., Kawai, Y., Isono, Y., Nakamura, Y., Nagahari, K., Murakami, K., Yasuda, T., Iwayanagi, T., Wagatsuma, M., Shiratori, A., Sudo, H., Hosoiri, T., Kaku, Y., Kodaira, H., Kondo, H., Sugawara, M., Takahashi, M., Kanda, K., Yokoi, T., Furuya, T., Kikkawa, E., Omura, Y., Abe, K., Kamihara, K., Katsuta, N., Sato, K., Tanikawa, M., Yamazaki, M., Ninomiya, K., Ishibashi, T., Yamashita, H., Murakawa, K., Fujimori, K., Tanai, H., Kimata, M., Watanabe, M., Hiraoka, S., Chiba, Y., Ishida, S., Ono, Y., Takiguchi, S., Watanabe, S., Yosida, M., Hotuta, T., Kusano, J., Kanehori, K., Takahashi-Fujii, A., Hara, H., Tanase, T. O., Nomura, Y., Togiya, S., Komai, F., Hara, R., Takeuchi, K., Arita, M., Imose, N., Musashino, K., Yuuki, H., Oshima, A., Sasaki, N., Aotsuka, S., Yoshikawa, Y., Matsunawa, H., Ichihara, T., Shiohata, N., Sano, S., Moriya, S., Momiyama, H., Satoh, N., Takami, S., Terashima, Y., Suzuki, O., Nakagawa, S., Senoh, A., Mizoguchi, H., Goto, Y., Shimizu, P., Wakebe, H., Hishigaki, H., Watanabe, T., Sugiyama, A., et al. (2004) Complete sequencing and characterization of 21,243 full-length human cDNAs, Nat. Genet. 36, 40-45.
35. Vekrellis, K., Ye, Z., Qiu, W. Q., Walsh, D., Hartley, D., Chesneau, V., Rosner, M. R., and Selkoe, D. J. (2000) Neurons regulate extracellular levels of amyloid β-protein via proteolysis by insulin-degrading enzyme, J. Neurosci. 20, 1657-1665.
36. La Voie, M. J., Fraering, P. C., Ostaszewski, B. L., Ye, W., Kimberly, W. T., Wolfe, M. S., and Selkoe, D. J. (2003) Assembly of the γ-secretase complex involves early formation of an intermediate subcomplex of Aph-1 and nicastrin, J. Biol. Chem. 278, 37213-37222.
37. Leissring, M. A., Lu, A., Condron, M. M., Teplow, D. B., Stein, R. L., Farris, W., and Selkoe, D. J. (2003) Kinetics of amyloid β-protein degradation determined by novel fluorescence- and fluorescence polarization-based assays, J. Biol. Chem. 278, 37314-37320.
38. Xia, W., Ray, W. J., Ostaszewski, B. L., Rahmati, T., Kimberly, W. T., Wolfe, M. S., Zhange, J., Goate, A. M., and Selkoe, D. J. (2000) Presenilin complexes with the C-terminal fragments of amyloid precursor protein at the sites of amyloid β-protein generation, Proc. Natl. Acad. Sci. U.S.A. 97, 9299-9304.
39. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., and Bairoch, A. (2003) ExPASy: The proteomics server for in-depth protein knowledge and analysis, Nucleic Acids Res. 31, 3784-3788.
40. Soltys, B. J., and Gupta, R. S. (1996) Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells, Exp. Cell Res. 222, 16-27.
41. Kuo, W.-L., Gehm, B. D., Rosner, M. R., Li, W., and Keller, G. (1994) Inducible expression and cellular localization of insulin-degrading enzyme in a stably transfected cell line, J. Biol. Chem. 269, 22599-22606.
42. Song, E. S., Juliano, M. A., Juliano, L., and Hersh, L. B. (2003) Substrate activation of insulin-degrading enzyme (insulysin). A potential target for drug development, J. Biol. Chem. 278, 49789-49794.
43. Chesneau, V., and Rosner, M. R. (2000) Functional human insulin-degrading enzyme can be expressed in bacteria, Protein Expression Purif. 19, 91-98.
44. Lustbader, J. W., Cirilli, M., Lin, C., Xu, H. W., Takuma, K., Wang, N., Caspersen, C., Chen, X., Pollak, S., Chaney, M., Trinchese, F., Liu, S., Gunn-Moore, F., Lue, L. F., Walker, D. G., Kuppusamy, P., Zewier, Z. L., Arancio, O., Stern, D., Yan, S. S., and Wu, H. (2004) ABAD directly links Aβ to mitochondrial toxicity in Alzheimer's disease, Science 304, 448-452.
45. Conne, B., Stutz, A., and Vassalli, J. D. (2000) The 3′ untranslated region of messenger RNA: A molecular 'hotspot' for pathology? Nat. Med. 6, 637-641.
46. Hamel, F. G., Bennett, R. G., and Duckworth, W. C. (1998) Regulation of multicatalytic enzyme activity by insulin and the insulin-degrading enzyme, Endocrinology 139, 4061-4066.
47. Kupfer, S. R., Wilson, E. M., and French, F. S. (1994) Androgen and glucocorticoid receptors interact with insulin degrading enzyme, J. Biol. Chem. 269, 20622-20628.
48. Takai, D., and Jones, P. A. (2002) Comprehensive analysis of CpG islands in human chromosomes 21 and 22, Proc. Natl. Acad. Sci. U.S.A. 99, 3740-3745.
49. Authier, F., Bergeron, J. J., Ou, W. J., Rachubinski, R. A., Posner, B. I., and Walton, P. A. (1995) Degradation of the cleaved leader peptide of thiolase by a peroxisomal proteinase, Proc. Natl. Acad. Sci. U.S.A. 92, 3859-3863.
50. Schmitz, A., Schneider, A., Kummer, M. P., and Herzog, V. (2004) Endoplasmic reticulum-localized amyloid β-peptide is degraded in the cytosol by two distinct degradation pathways, Traffic 5, 89-101.
51. Ho, L., Qin, W., Pompl, P. N., Xiang, Z., Wang, J., Zhao, Z., Peng, Y., Cambareri, G., Rocher, A., Mobbs, C. V., Hof, P. R., and Pasinetti, G. M. (2004) Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease, FASEB J. 18, 902-904.
52. Cook, D. G., Leverenz, J. B., McMillan, P. J., Kulstad, J. J., Ericksen, S., Roth, R. A., Schellenberg, G. D., Jin, L. W., Kovacina, K. S., and Craft, S. (2003) Reduced hippocampal insulin-degrading enzyme in late-onset Alzheimer's disease is associated with the apolipoprotein E-ε4 allele, Am. J. Pathol. 162, 313-319.
53. Perez, A;., Morelli, L., Cresto, J. C., and Castano, E. M. (2000) Degradation of soluble amyloid β-peptides 1-40, 1-42, and the Dutch variant 1-40Q by insulin degrading enzyme from Alzheimer disease and control brains, Neurochem. Res. 25, 247-255.