Developmental regulation of synthesis and dimerization of the amyloidogenic protease inhibitor cystatin C in the Hematopoietic System

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9730-9740

  Xu, Yuekang ^a,b   Lindemann, Petra ^a   Vega Ramos, Javier ^c   Zhang, Jian Guo ^a   Villadangos, Jose A ^a,b,c  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; CYTOLOGY; DIAGNOSIS; DIMERS; DISEASES; ENZYME ACTIVITY; INDUSTRIAL POISONS; MACROPHAGES;

CYSTEINE PROTEASE INHIBITORS; ENDOPLASMIC RETICULUM; EXTRACELLULAR CONCENTRATION; HEMATOPOIETIC SYSTEMS; INFLAMMATORY PROCESS; INTRACELLULAR CONCENTRATION; PROTEASE ACTIVITIES; REACTIVE OXYGEN SPECIES;

DIMERIZATION;

CYSTATIN C; DIMER; MONOMER; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DIMERIZATION; ENDOPLASMIC RETICULUM; HEMATOPOIETIC CELL; HEMATOPOIETIC SYSTEM; IN VIVO STUDY; MACROPHAGE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION;

AMYLOIDOSIS; DENDRITIC CELLS; MACROPHAGES; PROTEASE INHIBITOR; PROTEIN FOLDING; REACTIVE OXYGEN SPECIES (ROS); VASCULAR ANGIOPATHY;

ANIMALS; CYSTATIN C; DENDRITIC CELLS; ENDOPLASMIC RETICULUM; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; INFLAMMATION; MACROPHAGES; MICE; MICE, MUTANT STRAINS; MITOCHONDRIA; PROTEIN BIOSYNTHESIS; PROTEIN MULTIMERIZATION; REACTIVE OXYGEN SPECIES;

EID: 84898069682     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.538041     Document Type: Article

References (49)

1. Abrahamson, M., Alvarez-Fernandez, M., and Nathanson, C. M. (2003) Cystatins. Biochem. Soc. Symp. 70, 179-199
2. Keppler, D. (2006) Towards novel anti-cancer strategies based on cystatin function. Cancer Lett 235, 159-176
3. Shi, G. P., Sukhova, G. K., Grubb, A., Ducharme, A., Rhode, L. H., Lee, R. T., Ridker, P. M., Libby, P., and Chapman, H. A. (1999) Cystatin C deficiency in human atherosclerosis and aortic aneurysms. J. Clin. Invest. 104, 1191-1197
4. Liu, J., Sukhova, G. K., Sun, J. S., Xu, W. H., Libby, P., and Shi, G. P. (2004) Lysosomal cysteine proteases in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 24, 1359-1366
5. Rokadia, H. K., and Agarwal, S. (2012) Serum cystatin C and emphysema: results from the National Health and Nutrition Examination Survey (NHANES). Lung 190, 283-290
6. Bird, P. I., Trapani, J. A., and Villadangos, J. A. (2009) Endolysosomal proteases and their inhibitors in immunity. Nat. Rev. Immunol. 9, 871-882
7. Grubb, A. (2010) Non-invasive estimation of glomerular filtration rate (GFR). The Lund model: simultaneous use of cystatin C-and creatinine-based GFR-prediction equations, clinical data and an internal quality check. Scand. J. Clin. Lab. Invest. 70, 65-70
8. Shlipak, M. G., Matsushita, K., Ärnlöv, J., Inker, L. A., Katz, R., Polking-horne, K. R., Rothenbacher, D., Sarnak, M. J., Astor, B. C., Coresh, J., Levey, A. S., Gansevoort, R. T., and CKD Prognosis Consortium (2013) Cystatin C versus creatinine in determining risk based on kidney function. N. Engl. J. Med. 369, 932-943
9. Smith, E. R. (2013) Cystatin C. More than a filtration marker? Atherosclerosis 230, 73-75
10. Tamura, T., Thotakura, P., Tanaka, T. S., Ko, M. S., and Ozato, K. (2005) Identification of target genes and a unique cis element regulated by IRF-8 in developing macrophages. Blood 106, 1938-1947
11. Xu, Y., Schnorrer, P., Proietto, A., Kowalski, G., Febbraio, M. A., Acha-Orbea, H., Dickins, R. A., and Villadangos, J. A. (2011) IL-10 controls cystatin C synthesis and blood concentration in response to inflammation through regulation ofIFN regulatory factor 8 expression. J. Immunol. 186, 3666-3673
12. Kaur, G., and Levy, E. (2012) Cystatin C in Alzheimer's disease. Front. Mol. Neurosci. 5, 79
13. Janowski, R., Kozak, M., Jankowska, E., Grzonka, Z., Grubb, A., Abraham-son, M., and Jaskolski, M. (2001) Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping. Nat. Struct. Biol. 8, 316-320
14. Wahlbom, M., Wang, X., Lindström, V., Carlemalm, E., Jaskolski, M., and Grubb, A. (2007) Fibrillogenic oligomers of human cystatin C are formed by propagated domain swapping. J. Biol. Chem. 282, 18318-18326
15. Mi, W., Jung, S. S., Yu, H., Schmidt, S. D., Nixon, R. A., Mathews, P. M., Tagliavini, F., and Levy, E. (2009) Complexes of amyloid-/3 and cystatin C in the human central nervous system. J. Alzheimers Dis. 18, 273-280
16. Palsdottir, A., Abrahamson, M., Thorsteinsson, L., Arnason, A., Olafsson, I., Grubb, A., and Jensson, O. (1988) Mutation in cystatin C gene causes hereditary brain haemorrhage. Lancet 2, 603-604
17. Mi, W., Pawlik, M., Sastre, M., Jung, S. S., Radvinsky, D. S., Klein, A. M., Sommer, J., Schmidt, S. D., Nixon, R. A., Mathews, P. M., and Levy, E. (2007) Cystatin C inhibits amyloid-beta deposition in Alzheimer's disease mouse models. Nat Genet. 39, 1440-1442
18. Levy, E., Jaskolski, M., and Grubb, A. (2006) The role of cystatin C in cerebral amyloid angiopathy and stroke: cell biology and animal models. Brain Pathol. 16, 60-70
19. Huh, C. G., Håkansson, K., Nathanson, C. M., Thorgeirsson, U. P., Jons-son, N, Grubb, A., Abrahamson, M., and Karlsson, S. (1999) Decreased metastatic spread in mice homozygous for a null allele of the cystatin C protease inhibitor gene. Mol. Pathol. 52, 332-340
20. Vremec, D., Pooley, J., Hochrein, H., Wu, L., andShortman, K. (2000) CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164, 2978-2986
21. Xu, Y., Zhan, Y., Lew, A. M., Naik, S. H, and Kershaw, M. H. (2007) Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J. Immunol. 179, 7577-7584
22. Zhan, Y., Vega-Ramos, J., Carrington, E. M., Villadangos, J. A., Lew, A. M., and Xu, Y. (2012) The inflammatory cytokine, GM-CSF, alters the developmental outcome of murine dendritic cells. Eur. J. Immunol. 42, 2889-2900
23. + T cells in response to viral infections of the lung and skin. Eur. J. Immunol. 36, 327-335
24. Villadangos, J. A., Riese, R. J., Peters, C, Chapman, H. A., and Ploegh, H. L. (1997) Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J. Exp. Med. 186, 549-560
25. Xu, Y., Huntington, N. D., Harder, K. W., Nandurkar, H, Hibbs, M. L., and Tarlinton, D. M. (2012) Phosphatidylinositol-3 kinase activity in B cells is negatively regulated by Lyn tyrosine kinase. Immunol. Cell Biol. 90, 903-911
26. Warfel, A. H, Zucker-Franklin, D., Frangione, B., and Ghiso, J. (1987) Constitutive secretion of cystatin C (7-trace) by monocytes and macrophages and its down-regulation after stimulation. J. Exp. Med. 166, 1912-1917
27. Henskens, Y. M., Veerman, E. C, and Nieuw Amerongen, A. V. (1996) Cystatins in health and disease. Biol. Chem. Hoppe Seyler 377, 71-86
28. Gotoh, Y., and Cooper, J. A. (1998) Reactive oxygen species-and dimeriza-tion-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-a signal transduction. J. Biol. Chem. 273, 17477-17482
29. Wilson, N. S., El-Sukkari, D., Belz, G. T., Smith, C. M., Steptoe, R. J., Heath, W. R., Shortman, K., and Villadangos, J. A. (2003) Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102, 2187-2194
30. + and CD8~ dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174, 6592-6597
31. Keelan, J., Allen, N. J., Antcliffe, D., Pal, S., and Duchen, M. R. (2001) Quantitative imaging of glutathione in hippocampal neurons and glia in culture using monochlorobimane. J. Neurosci. Res. 66, 873-884
32. Murphy, M. P. (2009) How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13
33. Palsdottir, A., Helgason, A., Palsson, S., Bjornsson, H. T., Bragason, B. T., Gretarsdottir, S., Thorsteinsdottir, U., Olafsson, E., and Stefansson, K. (2008) A drastic reduction in the life span of cystatin C L68Q carriers due to life-style changes during the last two centuries. PLoS Genet. 4, e1000099
34. Bobryshev, Y. V. (2010) Dendritic cells and their role in atherogenesis. Lab. Invest. 90, 970-984
35. Terry, R. L., Getts, D. R., Deffrasnes, C, van Vreden, C, Campbell, I. L., and King, N. J. (2012) Inflammatory monocytes and the pathogenesis of viral encephalitis. J. Neuroinflammation 9, 270
36. Choi, J. H., Cheong, C, Dandamudi, D. B., Park, C. G., Rodriguez, A., Mehandru, S., Velinzon, K., Jung, I. H, Yoo, J. Y., Oh, G. T., and Steinman, R. M. (2011) Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity 35, 819-831
37. Rosenfeld, M. E. (1998) Inflammation, lipids, and free radicals: lessons learned from the atherogenic process. Semin. Reprod. Endocrinol. 16, 249-261
38. Sukhova, G. K., Wang, B., Libby, P., Pan, J. H, Zhang, Y., Grubb, A., Fang, K., Chapman, H. A., and Shi, G. P. (2005) Cystatin C deficiency increases elastic lamina degradation and aortic dilatation in apolipoprotein E-null mice. Circ. Res. 96, 368-375
39. Randers, E., and Erlandsen, E. J. (1999) Serum cystatin C as an endogenous marker of the renal function. A review. Clin. Chem. Lab. Med. 37, 389-395
40. Evangelopoulos, A. A., Vallianou, N. G., Bountziouka, V., Katsagoni, C., Bathrellou, E., Vogiatzakis, E. D., Bonou, M. S., Barbetseas, J., Avgerinos, P. C., and Panagiotakos, D. B. (2012) Association between serum cystatin C, monocytes and other inflammatory markers. Intern. Med. J. 42, 517-522
41. Ganda, A., Magnusson, M., Yvan-Charvet, L., Hedblad, B., Engström, G., Ai, D., Wang, T. J., Gerszten, R. E., Melander, O., and Tall, A. R. (2013) Mild renal dysfunction and metabolites tied to low HDL cholesterol are associated with monocytosis and atherosclerosis. Circulation 127, 988-996
42. Sun, B., Zhou, Y., Halabisky, B., Lo, I., Cho, S. H., Mueller-Steiner, S., Devidze, N., Wang, X., Grubb, A., and Gan, L. (2008) Cystatin C-cathepsin B axis regulates amyloid beta levels and associated neuronal deficits in an animal model of Alzheimer's disease. Neuron 60, 247-257
43. Nishiyama, K., Konishi, A., Nishio, C., Araki-Yoshida, K., Hatanaka, H., Kojima, M., Ohmiya, Y., Yamada, M., and Koshimizu, H. (2005) Expression of cystatin C prevents oxidative stress-induced death in PC12 cells. Brain Res. Bull. 67, 94-99
44. Tizon, B., Sahoo, S., Yu, H., Gauthier, S., Kumar, A. R., Mohan, P., Figliola, M., Pawlik, M., Grubb, A., Uchiyama, Y., Bandyopadhyay, U., Cuervo, A. M., Nixon, R. A., and Levy, E. (2010) Induction of autophagy by cystatin C: a mechanism that protects murine primary cortical neurons and neu-ronal cell lines. PLoS One 5, e9819
45. Nilsson, M., Wang, X., Rodziewicz-Motowidlo, S., Janowski, R., Lind-ström, V., Onnerfjord, P., Westermark, G., Grzonka, Z., Jaskolski, M., and Grubb, A. (2004) Prevention of domain swapping inhibits dimerization and amyloid fibril formation of cystatin C: use of engineered disulfide bridges, antibodies, and carboxymethylpapain to stabilize the monomeric form of cystatin C. J. Biol. Chem. 279, 24236-24245
46. Merz, G. S., Benedikz, E., Schwenk, V., Johansen, T. E., Vogel, L. K., Rush-brook, J. I., and Wisniewski, H. M. (1997) Human cystatin C forms an inactive dimer during intracellular trafficking in transfected CHO cells. J. Cell Physiol. 173, 423-432
47. Xie, L., Terrand, J., Xu, B., Tsaprailis, G., Boyer, J., and Chen, Q. M. (2010) CystatinC increases incardiac injury:a rolein extracellular matrix protein modulation. Cardiovasc. Res. 87, 628-635
48. El-Sukkari, D., Wilson, N. S., Hakansson, K., Steptoe, R. J., Grubb, A., Shortman, K., and Villadangos, J. A. (2003) The protease inhibitor cystatin C is differentially expressed among dendritic cell populations, but does not control antigen presentation. J. Immunol. 171, 5003-5011
49. Kim, C. C., and Lanier, L. L. (2013) Beyond the transcriptome: completion of act oneofthe immunological genome project.Curr. Opin. Immunol.25, 593-597