The molecular basis for development of proinflammatory autoantibodies to progranulin

Journal of Autoimmunity

Volumn 61, Issue , 2015, Pages 17-28

  Thurner, Lorenz ^a   Fadle, Natalie ^a   Regitz, Evi ^a   Kemele, Maria ^a   Klemm, Philipp ^a   Zaks, Marina ^a   Stöger, Elisabeth ^a   Bette, Birgit ^a   Carbon, Gabi ^a   Zimmer, Vincent ^a   Assmann, Gunter ^a   Murawski, Niels ^a   Kubuschok, Boris ^a   Held, Gerhard ^a   Preuss, Klaus Dieter ^a   Pfreundschuh, Michael ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Alternative conversion; DR3; Hyperphosphorylation of Ser81; Neoantigen; PKC 1; PP1; Progranulin; Proinflammatory autoantibody; TNFR1 2

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ALKALINE PHOSPHATASE; AUTOANTIBODY; EPITOPE; PROGRANULIN; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA 1; SERINE; UNCLASSIFIED DRUG; DEATH RECEPTOR 3; GRN PROTEIN, HUMAN; ISOPROTEIN; PROTEIN PRECURSOR; SIGNAL PEPTIDE; TNFRSF25 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

ADAPTIVE IMMUNITY; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; CYTOTOXICITY ASSAY; FEMALE; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; ISOELECTRIC FOCUSING; PHOSPHORYLATION; PHOSPHORYLATION AND DEPHOSPHORYLATION; PRIORITY JOURNAL; SEROCONVERSION; SITE DIRECTED MUTAGENESIS; ANIMAL; BINDING SITE; CELL LINE; FLOW CYTOMETRY; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; AUTOANTIBODIES; BINDING SITES; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN KINASE C BETA; PROTEIN PRECURSORS; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 25; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; SERINE;

EID: 84937523818     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2015.05.002     Document Type: Article

References (44)

1. Thurner L., Preuss K.D., Fadle N., Regitz E., Klemm P., Zaks M., Kemele M., Hasenfus A., Csernok E., Gross W.L., Pasquali J.L., Martin T., Bohle R.M., Pfreundschuh M. Progranulin antibodies in autoimmune diseases. J. Autoimmun. 2013 May, 42:29-38. [Epub 2012 Nov 11]. 10.1016/j.jaut.2012.10.003.
2. Thurner L., Zaks M., Preuss K.D., Fadle N., Regitz E., Ong M.F., Pfreundschuh M., Assmann G. Progranulin antibodies entertain a proinflammatory environment in a subgroup of patients with psoriatic arthritis. Arthritis Res. Ther. 2013, 15:R211.
3. Thurner L., Stoger E., Fadle N., Klemm P., Regitz E., Kemele M., Bette B., Held G., Dauer M., Lammert F., Preuss K.D., Zimmer V., Pfreundschuh M. Proinflammatory progranulin antibodies in inflammatory bowel diseases. Dig. Dis. Sci. 2014.
4. Toh H., Chitramuthu B.P., Bennett H.P., Bateman A. Structure, function, and mechanism of progranulin; the brain and beyond. J. Mol. Neurosci. 2011, 45:538-548.
5. Bateman A., Bennett H.P. The granulin gene family: from cancer to dementia. Bioessays 2009, 31:1245-1254.
6. He Z., Ong C.H., Halper J., Bateman A. Progranulin is a mediator of the wound response. Nat. Med. 2003, 9:225-229.
7. Ryan C.L., Baranowski D.C., Chitramuthu B.P., Malik S., Li Z., Cao M., Minotti S., Durham H.D., Kay D.G., Shaw C.A., Bennett H.P., Bateman A. Progranulin is expressed within motor neurons and promotes neuronal cell survival. BMC Neurosci. 2009, 10:130.
8. Baker M., Mackenzie I.R., Pickering-Brown S.M., Gass J., Rademakers R., Lindholm C., Snowden J., Adamson J., Sadovnick A.D., Rollinson S., Cannon A., Dwosh E., Neary D., Melquist S., Richardson A., Dickson D., Berger Z., Eriksen J., Robinson T., Zehr C., Dickey C.A., Crook R., McGowan E., Mann D., Boeve B., Feldman H., Hutton M. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 2006, 442:916-919.
9. Galimberti D., D'Addario C., Dell'osso B., Fenoglio C., Marcone A., Cerami C., Cappa S.F., Palazzo M.C., Arosio B., Mari D., Maccarrone M., Bresolin N., Altamura A.C., Scarpini E. Progranulin gene (GRN) promoter methylation is increased in patients with sporadic frontotemporal lobar degeneration. Neurol. Sci. 2012.
10. Ong C.H., Bateman A. Progranulin (granulin-epithelin precursor, PC-cell derived growth factor, acrogranin) in proliferation and tumorigenesis. Histol. Histopathol. 2003, 18:1275-1288.
11. Gobel M., Eisele L., Mollmann M., Huttmann A., Johansson P., Scholtysik R., Bergmann M., Busch R., Dohner H., Hallek M., Seiler T., Stilgenbauer S., Klein-Hitpass L., Duhrsen U., Durig J. Progranulin is a novel independent predictor of disease progression and overall survival in chronic lymphocytic leukemia. PLoS One 2013, 8:e72107.
12. Cheung P.F., Cheng C.K., Wong N.C., Ho J.C., Yip C.W., Lui V.C., Cheung A.N., Fan S.T., Cheung S.T. Granulin-epithelin precursor is an oncofetal protein defining hepatic cancer stem cells. PLoS One 2011, 6:e28246.
13. Frampton G., Invernizzi P., Bernuzzi F., Pae H.Y., Quinn M., Horvat D., Galindo C., Huang L., McMillin M., Cooper B., Rimassa L., DeMorrow S. Interleukin-6-driven progranulin expression increases cholangiocarcinoma growth by an Akt-dependent mechanism. Gut 2012, 61:268-277.
14. Ho J.C., Ip Y.C., Cheung S.T., Lee Y.T., Chan K.F., Wong S.Y., Fan S.T. Granulin-epithelin precursor as a therapeutic target for hepatocellular carcinoma. Hepatology 2008, 47:1524-1532.
15. Kessenbrock K., Frohlich L., Sixt M., Lammermann T., Pfister H., Bateman A., Belaaouaj A., Ring J., Ollert M., Fassler R., Jenne D.E. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J. Clin. Invest. 2008, 118:2438-2447.
16. Zhu J., Nathan C., Jin W., Sim D., Ashcroft G.S., Wahl S.M., Lacomis L., Erdjument-Bromage H., Tempst P., Wright C.D., Ding A. Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 2002, 111:867-878.
17. Tang W., Lu Y., Tian Q.Y., Zhang Y., Guo F.J., Liu G.Y., Syed N.M., Lai Y., Lin E.A., Kong L., Su J., Yin F., Ding A.H., Zanin-Zhorov A., Dustin M.L., Tao J., Craft J., Yin Z., Feng J.Q., Abramson S.B., Yu X.P., Liu C.J. The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 2011, 332:478-484.
18. Liu C., Li X.X., Gao W., Liu W., Liu D.S. Progranulin-derived Atsttrin directly binds to TNFRSF25 (DR3) and inhibits TNF-like ligand 1A (TL1A) activity. PLoS One 2014, 9:e92743.
19. Lai Y., Yu X.P., Zhang Y., Tian Q., Song H., Mucignat M.T., Perris R., Samuels J., Krasnokutsky S., Attur M., Greenberg J.D., Abramson S.B., Di Cesare P.E., Liu C.J. Enhanced COMP catabolism detected in serum of patients with arthritis and animal disease models through a novel capture ELISA. Osteoarthr. Cartil. 2012, 20:854-862.
20. Guo F., Lai Y., Tian Q., Lin E.A., Kong L., Liu C. Granulin-epithelin precursor binds directly to ADAMTS-7 and ADAMTS-12 and inhibits their degradation of cartilage oligomeric matrix protein. Arthritis Rheum. 2010, 62:2023-2036.
21. Zhao Y.P., Tian Q.Y., Liu C.J. Progranulin deficiency exaggerates, whereas progranulin-derived Atsttrin attenuates, severity of dermatitis in mice. FEBS Lett. 2013, 587:1805-1810.
22. Egashira Y., Suzuki Y., Azuma Y., Takagi T., Mishiro K., Sugitani S., Tsuruma K., Shimazawa M., Yoshimura S., Kashimata M., Iwama T., Hara H. The growth factor progranulin attenuates neuronal injury induced by cerebral ischemia-reperfusion through the suppression of neutrophil recruitment. J. Neuroinflamm. 2013, 10:105.
23. Liu C.J. Progranulin: a promising therapeutic target for rheumatoid arthritis. FEBS Lett. 2011, 585:3675-3680.
24. Liu C.J., Bosch X. Progranulin: a growth factor, a novel TNFR ligand and a drug target. Pharmacol. Ther. 2012, 133:124-132.
25. Neumann F., Wagner C., Preuss K.D., Kubuschok B., Schormann C., Stevanovic S., Pfreundschuh M. Identification of an epitope derived from the cancer testis antigen HOM-TES-14/SCP1 and presented by dendritic cells to circulating CD4+ T cells. Blood 2005, 106:3105-3113.
26. Grass S., Preuss K.D., Ahlgrimm M., Fadle N., Regitz E., Pfoehler C., Murawski N., Pfreundschuh M. Association of a dominantly inherited hyperphosphorylated paraprotein target with sporadic and familial multiple myeloma and monoclonal gammopathy of undetermined significance: a case-control study. Lancet Oncol. 2009, 10:950-956.
27. Held G., Wadle A., Dauth N., Stewart-Jones G., Sturm C., Thiel M., Zwick C., Dieckmann D., Schuler G., Hoogenboom H.R., Levy F., Cerundolo V., Pfreundschuh M., Renner C. MHC-peptide-specific antibodies reveal inefficient presentation of an HLA-A*0201-restricted, Melan-A-derived peptide after active intracellular processing. Eur. J. Immunol. 2007, 37:2008-2017.
28. Preuss K.D., Pfreundschuh M., Fadle N., Regitz E., Raudies S., Murwaski N., Ahlgrimm M., Bittenbring J., Klotz M., Schafer K.H., Held G., Neumann F., Grass S. Hyperphosphorylation of autoantigenic targets of paraproteins is due to inactivation of PP2A. Blood 2011, 118:3340-3346.
29. de Haard H.J., van N.N., Reurs A., Hufton S.E., Roovers R.C., Henderikx P., de Bruine A.P., Arends J.W., Hoogenboom H.R. A large non-immunized human Fab fragment phage library that permits rapid isolation and kinetic analysis of high affinity antibodies. J. Biol. Chem. 1999, 274:18218-18230.
30. Merck KGaA, Darmstadt G Calbiochem Inhibitor Sourcebook 2009.
31. Tanaka M., Sagawa S., Hoshi J., Shimoma F., Matsuda I., Sakoda K., Sasase T., Shindo M., Inaba T. Synthesis of anilino-monoindolylmaleimides as potent and selective PKCbeta inhibitors. Bioorg Med. Chem. Lett. 2004, 14:5171-5174.
32. Grass S., Preuss K.D., Thome S., Weisenburger D.D., Witt V., Lynch J., Zettl F., Trumper L., Fadle N., Regitz E., Lynch H., Pfreundschuh M. Paraproteins of familial MGUS/multiple myeloma target family-typical antigens: hyperphosphorylation of autoantigens is a consistent finding in familial and sporadic MGUS/MM. Blood 2011, 118:635-637.
33. Schellekens G.A., de Jong B.A., van den Hoogen F.H., van de Putte L.B., van Venrooij W.J. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J. Clin. Invest. 1998, 101:273-281.
34. van Venrooij W.J., Pruijn G.J. Citrullination: a small change for a protein with great consequences for rheumatoid arthritis. Arthritis Res. 2000, 2:249-251.
35. Zamvil S.S., Mitchell D.J., Moore A.C., Kitamura K., Steinman L., Rothbard J.B. T-cell epitope of the autoantigen myelin basic protein that induces encephalomyelitis. Nature 1986, 324:258-260.
36. Arentz-Hansen H., Korner R., Molberg O., Quarsten H., Vader W., Kooy Y.M., Lundin K.E., Koning F., Roepstorff P., Sollid L.M., McAdam S.N. The intestinal T cell response to alpha-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J. Exp. Med. 2000, 191:603-612.
37. Neugebauer K.M., Merrill J.T., Wener M.H., Lahita R.G., Roth M.B. SR proteins are autoantigens in patients with systemic lupus erythematosus. Importance of phosphoepitopes. Arthritis Rheum. 2000, 43:1768-1778.
38. Utz P.J., Hottelet M., Schur P.H., Anderson P. Proteins phosphorylated during stress-induced apoptosis are common targets for autoantibody production in patients with systemic lupus erythematosus. J. Exp. Med. 1997, 185:843-854.
39. Preuss K.D., Pfreundschuh M., Ahlgrimm M., Fadle N., Regitz E., Murawski N., Grass S. A frequent target of paraproteins in the sera of patients with multiple myeloma and MGUS. Int. J. Cancer 2009, 125:656-661.
40. Grass S., Preuss K.D., Wikowicz A., Terpos E., Ziepert M., Nikolaus D., Yang Y., Fadle N., Regitz E., Dimopoulos M.A., Treon S.P., Hunter Z.R., Pfreundschuh M. Hyperphosphorylated paratarg-7: a new molecularly defined risk factor for monoclonal gammopathy of undetermined significance of the IgM type and Waldenstrom macroglobulinemia. Blood 2011, 117:2918-2923.
41. Bai X.H., Wang D.W., Kong L., Zhang Y., Luan Y., Kobayashi T., Kronenberg H.M., Yu X.P., Liu C.J. ADAMTS-7, a direct target of PTHrP, adversely regulates endochondral bone growth by associating with and inactivating GEP growth factor. Mol. Cell. Biol. 2009, 29:4201-4219.
42. Suh H.S., Choi N., Tarassishin L., Lee S.C. Regulation of progranulin expression in human microglia and proteolysis of progranulin by matrix metalloproteinase-12 (MMP-12). PLoS One 2012, 7:e35115.
43. Butler G.S., Dean R.A., Tam E.M., Overall C.M. Pharmacoproteomics of a metalloproteinase hydroxamate inhibitor in breast cancer cells: dynamics of membrane type 1 matrix metalloproteinase-mediated membrane protein shedding. Mol. Cell. Biol. 2008, 28:4896-4914.
44. Wang J., Van D.P., Cruchaga C., Gitcho M.A., Vidal J.M., Seijo-Martinez M., Wang L., Wu J.Y., Robberecht W., Goate A. Pathogenic cysteine mutations affect progranulin function and production of mature granulins. J. Neurochem. 2010, 112:1305-1315.