Human high temperature requirement serine protease A1 (HTRA1) degrades tau protein aggregates

Journal of Biological Chemistry

Volumn 287, Issue 25, 2012, Pages 20931-20941

  Tennstaedt, Annette ^a   Pöpsel, Simon ^a   Truebestein, Linda ^a   Hauske, Patrick ^a   Brockmann, Anke ^a   Schmidt, Nina ^a   Irle, Inga ^a   Sacca, Barbara ^b   Niemeyer, Christof M ^b   Brandt, Roland ^c   Ksiezak Reding, Hanna ^d   Tirniceriu, Anca Laura ^e   Egensperger, Rupert ^e   Baldi, Alfonso ^f   Dehmelt, Leif ^g   Kaiser, Markus ^a   Huber, Robert ^a,b,h,i   Clausen, Tim ^j   Ehrmanna, Michael ^a,i  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b TU DORTMUND UNIVERSITY   (Germany)

^c UNIVERSITY OF OSNABRÜCK   (Germany)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MUNICH   (Germany)

^f SECOND UNIVERSITY OF NAPLES   (Italy)

^g MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^h MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

ⁱ CARDIFF UNIVERSITY   (United Kingdom)

^j RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ELEVATED LEVEL; HIGH TEMPERATURE; HTRA PROTEASE; KEY ELEMENTS; MISFOLDED PROTEINS; NEUROFIBRILLARY TANGLES; NEUROLOGICAL DISORDERS; NEURONAL CELL; PROTEIN AGGREGATES; PROTEIN QUALITY CONTROL; SERINE PROTEASE; TAU PROTEINS;

AMINO ACIDS; PROTEIN FOLDING; PROTEINS; QUALITY ASSURANCE; QUALITY CONTROL;

AGGREGATES;

HIGH TEMPERATURE REQUIREMENT SERINE PROTEASE A1; MESSENGER RNA; SERINE PROTEINASE; TAU PROTEIN; THIOFLAVINE; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOACCUMULATION; CONTROLLED STUDY; DEGRADATION KINETICS; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME DEGRADATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE; GENETIC TRANSFECTION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MASS SPECTROMETRY; MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NERVE CELL; NEUROFIBRILLARY TANGLE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENILE PLAQUE; SEQUENCE ANALYSIS; UPREGULATION;

BRAIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; NERVE TISSUE PROTEINS; NEURITES; PROTEIN FOLDING; PROTEOLYSIS; SERINE ENDOPEPTIDASES; TAU PROTEINS; TAUOPATHIES;

EID: 84862291060     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.316232     Document Type: Article

References (62)

1. Clausen, T., Southan, C., and Ehrmann, M. (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol. Cell 10, 443-455 (Pubitemid 35284166)
2. Clausen, T., Kaiser, M., Huber, R., and Ehrmann, M. (2011) HTRA proteases: regulated proteolysis in protein quality control. Nat. Rev. Mol. Cell Biol. 12, 152-162
3. Kley, J., Schmidt, B., Boyanov, B., Stolt-Bergner, P. C., Kirk, R., Ehrmann, M., Knopf, R. R., Naveh, L., Adam, Z., and Clausen, T. (2011) Structural adaptation of the plant protease Deg1 to repair photosystem II during light exposure. Nat. Struct. Mol. Biol. 18, 728-731
4. Sawa, J., Malet, H., Krojer, T., Canellas, F., Ehrmann, M., and Clausen, T. (2011) Molecular adaptation of the DegQ protease to exert protein quality control in the bacterial cell envelope. J. Biol. Chem. 286, 30680-30690
5. Merdanovic, M., Clausen, T., Kaiser, M., Huber, R., and Ehrmann, M. (2011) Protein quality control in the bacterial periplasm. Annu. Rev. Microbiol. 65, 149-168
6. Isaac, D. D., Pinkner, J. S., Hultgren, S. J., and Silhavy, T. J. (2005) The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. Proc. Natl. Acad. Sci. U.S.A. 102, 17775-17779 (Pubitemid 41803573)
7. Ehrmann, M., and Clausen, T. (2004) Proteolysis as a regulatory mechanism. Annu. Rev. Genet. 38, 709-724 (Pubitemid 40013742)
8. Wilken, C., Kitzing, K., Kurzbauer, R., Ehrmann, M., and Clausen, T. (2004) Crystal structure of the DegS stress sensor: how a PDZ domain recognizes misfolded protein and activates a protease. Cell 117, 483-494 (Pubitemid 38610233)
9. Spiess, C., Beil, A., and Ehrmann, M. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97, 339-347 (Pubitemid 29214590)
10. Truebestein, L., Tennstaedt, A., Mönig, T., Krojer, T., Canellas, F., Kaiser, M., Clausen, T., and Ehrmann, M. (2011) Substrate-induced remodeling of the active site regulates human HTRA1 activity. Nat. Struct. Mol. Biol. 18, 386-388
11. Krojer, T., Sawa, J., Schäfer, E., Saibil, H. R., Ehrmann, M., and Clausen, T. (2008) Structural basis for the regulated protease and chaperone function of DegP. Nature 453, 885-890 (Pubitemid 351832567)
12. Jones, A., Kumar, S., Zhang, N., Tong, Z., Yang, J. H., Watt, C., Anderson, J., Amrita, Fillerup, H., McCloskey, M., Luo, L., Yang, Z., Ambati, B., Marc, R., Oka, C., Zhang, K., and Fu, Y. (2011) Increased expression of multi-functional serine protease, HTRA1, in retinal pigment epithelium induces polypoidal choroidal vasculopathy in mice. Proc. Natl. Acad. Sci. U.S.A. 108, 14578-14583
13. Vierkotten, S., Muether, P. S., and Fauser, S. (2011) Overexpression of HTRA1 leads to ultrastructural changes in the elastic layer of Bruch's membrane via cleavage of extracellular matrix components. PLoS ONE 6, e22959
14. Grau, S., Richards, P. J., Kerr, B., Hughes, C., Caterson, B., Williams, A. S., Junker, U., Jones, S. A., Clausen, T., and Ehrmann, M. (2006) The role of human HtrA1 in arthritic disease. J. Biol. Chem. 281, 6124-6129 (Pubitemid 43847541)
15. Tsuchiya, A., Yano, M., Tocharus, J., Kojima, H., Fukumoto, M., Kawaichi, M., and Oka, C. (2005) Expression of mouse HtrA1 serine protease in normal bone and cartilage and its up-regulation in joint cartilage damaged by experimental arthritis. Bone 37, 323-336 (Pubitemid 41160491)
16. Chamberland, A., Wang, E., Jones, A. R., Collins-Racie, L. A., LaVallie, E. R., Huang, Y., Liu, L., Morris, E. A., Flannery, C. R., and Yang, Z. (2009) Identification of a novel HtrA1-susceptible cleavage site in human aggrecan: evidence for the involvement of HtrA1 in aggrecan proteolysis in vivo. J. Biol. Chem. 284, 27352-27359
17. Hadfield, K. D., Rock, C. F., Inkson, C. A., Dallas, S. L., Sudre, L., Wallis, G. A., Boot-Handford, R. P., and Canfield, A. E. (2008) HtrA1 inhibits mineral deposition by osteoblasts: requirement for the protease and PDZ domains. J. Biol. Chem. 283, 5928-5938
18. Chien, J., Ota, T., Aletti, G., Shridhar, R., Boccellino, M., Quagliuolo, L., Baldi, A., and Shridhar, V. (2009) Serine protease HtrA1 associates with microtubules and inhibits cell migration. Mol. Cell. Biol. 29, 4177-4187
19. Clawson, G. A., Bui, V., Xin, P., Wang, N., and Pan, W. (2008) Intracellular localization of the tumor suppressor HtrA1/Prss11 and its association with HPV16 E6 and E7 proteins. J. Cell. Biochem. 105, 81-88
20. Campioni, M., Severino, A., Manente, L., Tuduce, I. L., Toldo, S., Caraglia, M., Crispi, S., Ehrmann, M., He, X., Maguire, J., De Falco, M., De Luca, A., Shridhar, V., and Baldi, A. (2010) The serine protease HtrA1 specifically interacts and degrades the tuberous sclerosis complex 2 protein. Mol. Cancer Res. 8, 1248-1260
21. Chien, J., He, X., and Shridhar, V. (2009) Identification of tubulins as substrates of serine protease HtrA1 by mixture-based oriented peptide library screening. J. Cell. Biochem. 107, 253-263
22. Chien, J., Campioni, M., Shridhar, V., and Baldi, A. (2009) HtrA serine proteases as potential therapeutic targets in cancer. Curr. Cancer Drug Targets 9, 451-468
23. Yang, Z., Camp, N. J., Sun, H., Tong, Z., Gibbs, D., Cameron, D. J., Chen, H., Zhao, Y., Pearson, E., Li, X., Chien, J., Dewan, A., Harmon, J., Bernstein, P. S., Shridhar, V., Zabriskie, N. A., Hoh, J., Howes, K., and Zhang, K. (2006)Avariant of the HTRA1 gene increases susceptibility to age-related macular degeneration. Science 314, 992-993 (Pubitemid 44749944)
24. Grau, S., Baldi, A., Bussani, R., Tian, X., Stefanescu, R., Przybylski, M., Richards, P., Jones, S. A., Shridhar, V., Clausen, T., and Ehrmann, M. (2005) Implications of the serine protease HtrA1 in amyloid precursor protein processing. Proc. Natl. Acad. Sci. U.S.A. 102, 6021-6026 (Pubitemid 40594248)
25. Milner, J. M., Patel, A., and Rowan, A. D. (2008) Emerging roles of serine proteinases in tissue turnover in arthritis. Arthritis Rheum. 58, 3644-3656
26. Hara, K., Shiga, A., Fukutake, T., Nozaki, H., Miyashita, A., Yokoseki, A., Kawata, H., Koyama, A., Arima, K., Takahashi, T., Ikeda, M., Shiota, H., Tamura, M., Shimoe, Y., Hirayama, M., Arisato, T., Yanagawa, S., Tanaka, A., Nakano, I., Ikeda, S., Yoshida, Y., Yamamoto, T., Ikeuchi, T., Kuwano, R., Nishizawa, M., Tsuji, S., and Onodera, O. (2009) Association ofHTRA1 mutations and familial ischemic cerebral small-vessel disease. N. Engl. J. Med. 360, 1729-1739
27. Hasenbein, S., Meltzer, M., Hauske, P., Kaiser, M., Huber, R., Clausen, T., and Ehrmann, M. (2010) Conversion of a regulatory into a degradative protease. J. Mol. Biol. 397, 957-966
28. Krojer, T., Pangerl, K., Kurt, J., Sawa, J., Stingl, C., Mechtler, K., Huber, R., Ehrmann, M., and Clausen, T. (2008) Interplay of PDZ and protease domain of DegP ensures efficient elimination of misfolded proteins. Proc. Natl. Acad. Sci. U.S.A. 105, 7702-7707 (Pubitemid 351872702)
29. Krojer, T., Sawa, J., Huber, R., and Clausen, T. (2010) HtrA proteases have a conserved activation mechanism that can be triggered by distinct molecular cues. Nat. Struct. Mol. Biol. 17, 844-852
30. Merdanovic, M., Mamant, N., Meltzer, M., Poepsel, S., Auckenthaler, A., Melgaard, R., Hauske, P., Nagel-Steger, L., Clarke, A. R., Kaiser, M., Huber, R., and Ehrmann, M. (2010) Determinants of structural and functional plasticity of a widely conserved protease chaperone complex. Nat. Struct. Mol. Biol. 17, 837-843
31. Morris, M., Maeda, S., Vossel, K., and Mucke, L. (2011) The many faces of tau. Neuron 70, 410-426
32. Brandt, R., Hundelt, M., and Shahani, N. (2005) Tau alteration and neuronal degeneration in tauopathies: mechanisms and models. Biochim. Biophys. Acta 1739, 331-354 (Pubitemid 40018549)
33. Eidenmüller, J., Fath, T., Hellwig, A., Reed, J., Sontag, E., and Brandt, R. (2000) Structural and functional implications of tau hyperphosphorylation: information from phosphorylation-mimicking mutated tau proteins. Biochemistry 39, 13166-13175
34. Roger, B., Al-Bassam, J., Dehmelt, L., Milligan, R. A., and Halpain, S. (2004) MAP2c, but not tau, binds and bundles F-actin via its microtubule binding domain. Curr. Biol. 14, 363-371 (Pubitemid 38431169)
35. Morgenstern, J. P., and Land, H. (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596
36. Fath, T., Eidenmüller, J., and Brandt, R. (2002) Tau-mediated cytotoxicity in a pseudohyperphosphorylation model of Alzheimer's disease. J. Neurosci. 22, 9733-9741 (Pubitemid 35332856)
37. Li, W., and Lee, V. M. (2006) Characterization of two VQIXXK motifs for tau fibrillization in vitro. Biochemistry 45, 15692-15701 (Pubitemid 46032489)
38. Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004) Image Processing with Image J. Biophotonics Int. 11, 36-42
39. Hauske, P., Meltzer, M., Ottmann, C., Krojer, T., Clausen, T., Ehrmann, M., and Kaiser, M. (2009) Selectivity profiling of DegP substrates and inhibitors. Bioorg. Med. Chem. 17, 2920-2924
40. Meltzer, M., Hasenbein, S., Hauske, P., Kucz, N., Merdanovic, M., Grau, S., Beil, A., Jones, D., Krojer, T., Clausen, T., Ehrmann, M., and Kaiser, M. (2008) Allosteric activation of HtrA protease DegP by stress signals during bacterial protein quality control. Angew. Chem. Int. Ed. Engl. 47, 1332-1334
41. Xia, S. J., Rajput, P., Strzelecki, D. M., and Barr, F. G. (2007) Analysis of genetic events that modulate the oncogenic and growth suppressive activities of the PAX3-FKHR fusion oncoprotein. Lab. Invest. 87, 318-325 (Pubitemid 46474564)
42. Severino, A., Campioni, M., Straino, S., Salloum, F. N., Schmidt, N., Herbrand, U., Frede, S., Toietta, G., Di Rocco, G., Bussani, R., Silvestri, F., Piro, M., Liuzzo, G., Biasucci, L. M., Mellone, P., Feroce, F., Capogrossi, M., Baldi, F., Fandrey, J., Ehrmann, M., Crea, F., Abbate, A., and Baldi, A. (2007) Identification of protein disulfide isomerase as a cardiomyocyte survival factor in ischemic cardiomyopathy. J. Am. Coll. Cardiol. 50, 1029-1037 (Pubitemid 47348226)
43. Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M., Crain, B. J., Brownlee, L. M., Vogel, F. S., Hughes, J. P., van Belle, G., and Berg, L. (1991) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486
44. Braak, H., Alafuzoff, I., Arzberger, T., Kretzschmar, H., and Del Tredici, K. (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 112, 389-404 (Pubitemid 44469160)
45. Yang, L. S., Gordon-Krajcer, W., and Ksiezak-Reding, H. (1997) Tau released from paired helical filaments with formic acid or guanidine is susceptible to calpain-mediated proteolysis. J. Neurochem. 69, 1548-1558 (Pubitemid 27406956)
46. Egensperger, R., Kösel, S., von Eitzen, U., and Graeber, M. B. (1998) Microglial activation in Alzheimer disease: association with APOE genotype. Brain Pathol. 8, 439-447 (Pubitemid 28308843)
47. Friedhoff, P., Schneider, A., Mandelkow, E. M., and Mandelkow, E. (1998) Rapid assembly of Alzheimer-like paired helical filaments from microtubule- associated protein tau monitored by fluorescence in solution. Biochemistry 37, 10223-10230 (Pubitemid 28366378)
48. Rissman, R. A., Poon, W. W., Blurton-Jones, M., Oddo, S., Torp, R., Vitek, M. P., LaFerla, F. M., Rohn, T. T., and Cotman, C. W. (2004) Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest. 114, 121-130 (Pubitemid 39071651)
49. Mercken, M., Grynspan, F., and Nixon, R. A. (1995) Differential sensitivity to proteolysis by brain calpain of adult human tau, fetal human tau and PHF-tau. FEBS Lett. 368, 10-14
50. Talanian, R. V., Quinlan, C., Trautz, S., Hackett, M. C., Mankovich, J. A., Banach, D., Ghayur, T., Brady, K. D., and Wong, W. W. (1997) Substrate specificities of caspase family proteases. J. Biol. Chem. 272, 9677-9682 (Pubitemid 27171628)
51. Crowther, R. A. (1991) Straight and paired helical filaments in Alzheimer disease have a common structural unit. Proc. Natl. Acad. Sci. U.S.A. 88, 2288-2292
52. Berriman, J., Serpell, L. C., Oberg, K. A., Fink, A. L., Goedert, M., and Crowther, R. A. (2003) Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-β structure. Proc. Natl. Acad. Sci. U.S.A. 100, 9034-9038 (Pubitemid 36899218)
53. Barghorn, S., Davies, P., and Mandelkow, E. (2004) Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on β-structure in the core domain. Biochemistry 43, 1694-1703 (Pubitemid 38200576)
54. Karring, H., Runager, K., Thøgersen, I. B., Klintworth, G. K., Højrup, P., and Enghild, J. J. (2012) Composition and proteolytic processing of corneal deposits associated with mutations in the TGFBI gene. Exp. Eye Res. 96, 163-170
55. Suzuki, Y., Imai, Y., Nakayama, H., Takahashi, K., Takio, K., and Takahashi, R. (2001) A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell 8, 613-621 (Pubitemid 32946938)
56. Beleford, D., Rattan, R., Chien, J., and Shridhar, V. (2010) High temperature requirement A3 (HtrA3) promotes etoposide- and cisplatin-induced cytotoxicity in lung cancer cell lines. J. Biol. Chem. 285, 12011-12027
57. Dentillo, D. B., Meola, J., Rosa e Silva, J. C., Giuliatti, S., Silva, W. A., Jr., Ferriani, R. A., and Martelli, L. (2010) Deregulation of LOXL1 and HTRA1 gene expression in endometriosis. Reprod. Sci. 17, 1016-1023
58. Yang, Z., Tong, Z., Chen, Y., Zeng, J., Lu, F., Sun, X., Zhao, C., Wang, K., Davey, L., Chen, H., London, N., Muramatsu, D., Salasar, F., Carmona, R., Kasuga, D., Wang, X., Bedell, M., Dixie, M., Zhao, P., Yang, R., Gibbs, D., Liu, X., Li, Y., Li, C., Campochiaro, B., Constantine, R., Zack, D. J., Campochiaro, P., Fu, Y., Li, D. Y., Katsanis, N., and Zhang, K. (2010) Genetic and functional dissection of HTRA1 and LOC387715 in age-related macular degeneration. PLoS Genet. 6, e1000836
59. Launay, S., Maubert, E., Lebeurrier, N., Tennstaedt, A., Campioni, M., Docagne, F., Gabriel, C., Dauphinot, L., Potier, M. C., Ehrmann, M., Baldi, A., and Vivien, D. (2008) HtrA1-dependent proteolysis of TGF-β controls both neuronal maturation and developmental survival. Cell Death Differ. 15, 1408-1416
60. Chien, J., Aletti, G., Baldi, A., Catalano, V., Muretto, P., Keeney, G. L., Kalli, K. R., Staub, J., Ehrmann, M., Cliby, W. A., Lee, Y. K., Bible, K. C., Hartmann, L. C., Kaufmann, S. H., and Shridhar, V. (2006) Serine protease HtrA1 modulates chemotherapy-induced cytotoxicity. J. Clin. Invest. 116, 1994-2004 (Pubitemid 44033323)
61. Spugnini, E. P., Cardillo, I., Verdina, A., Crispi, S., Saviozzi, S., Calogero, R., Nebbioso, A., Altucci, L., Cortese, G., Galati, R., Chien, J., Shridhar, V., Vincenzi, B., Citro, G., Cognetti, F., Sacchi, A., and Baldi, A. (2006) Piroxicam and cisplatin in a mouse model of peritoneal mesothelioma. Clin. Cancer Res. 12, 6133-6143 (Pubitemid 44703779)
62. Polur, I., Lee, P. L., Servais, J. M., Xu, L., and Li, Y. (2010) Role of HTRA1, a serine protease, in the progression of articular cartilage degeneration. Histol. Histopathol. 25, 599-608