A rare variant in human fibroblast activation protein associated with ER stress, loss of enzymatic function and loss of cell surface localisation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 7, 2014, Pages 1248-1259

  Osborne, Brenna ^a,b,f   Yao, Tsun Wen ^a,b   Wang, Xin Maggie ^a,b   Chen, Yiqian ^a,b,g   Kotan, L Damla ^e   Nadvi, Naveed A ^a,d   Herdem, Mustafa ^e   McCaughan, Geoffrey W ^a,b,c   Allen, John D ^a,b   Yu, Denise M T ^a,b,h   Topaloglu, A Kemal ^e   Gorrell, Mark D ^a,b,c  

^a CENTENARY INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e CUKUROVA UNIVERSITY   (Turkey)

^f GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^g WESTMEAD HOSPITAL   (Australia)

^h UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Dipeptidyl peptidase; Endoplasmic reticulum associated degradation; Endoplasmic reticulum stress; Fibroblast activation protein; Polymorphism; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; AMINO ACID; BORTEZOMIB; DIPEPTIDYL PEPTIDASE; FIBROBLAST ACTIVATION PROTEIN; INITIATION FACTOR 2ALPHA; PROTEIN; PROTEIN VARIANT; SER363LEU AMINO ACID; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANTIGEN BINDING; APOPTOSIS; ARTICLE; CATALYSIS; CELL LOSS; CELL SURFACE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; GENOTYPE; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN FIBROBLAST; UPREGULATION;

DIPEPTIDYL PEPTIDASE; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; FIBROBLAST ACTIVATION PROTEIN; POLYMORPHISM; UNFOLDED PROTEIN RESPONSE;

AMINO ACID SUBSTITUTION; APOPTOSIS; BLOTTING, WESTERN; BRACHYDACTYLY; CASE-CONTROL STUDIES; CELL MEMBRANE; CELLS, CULTURED; DEAFNESS; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; FIBROBLASTS; FLOW CYTOMETRY; GELATINASES; HUMANS; IMMUNOENZYME TECHNIQUES; INTELLECTUAL DISABILITY; MEMBRANE PROTEINS; MOUTH ABNORMALITIES; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; SKIN; SUBCELLULAR FRACTIONS; TOOTH ABNORMALITIES;

EID: 84899809867     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.03.015     Document Type: Article

References (64)

1. E.J. Hamson, F.M. Keane, S. Tholen, O. Schilling, and M.D. Gorrell Understanding fibroblast activation protein (FAP): substrates, activities, expression and targeting for cancer therapy Proteomics Clin. Appl. 8 2014 10.1002/prca.201300095 (in press)
2. K.N. Lee, K.W. Jackson, V.J. Christiansen, E.K. Dolence, and P.A. McKee Enhancement of fibrinolysis by inhibiting enzymatic cleavage of precursor alpha2-antiplasmin J. Thromb. Haemost. 9 2011 987 996
3. D.M.T. Yu, T.-W. Yao, S. Chowdhury, N.A. Nadvi, B. Osborne, W.B. Church, G.W. McCaughan, and M.D. Gorrell The dipeptidyl peptidase IV family in cancer and cell biology FEBS J. 277 2010 1126 1144
4. M.D. Gorrell First bite Nat. Struct. Biol. 10 2003 3 5
5. P. Garin-Chesa, L.J. Old, and W.J. Rettig Cell surface glycoprotein of reactive stromal fibroblasts as a potential antibody target in human epithelial cancers Proc. Natl. Acad. Sci. U. S. A. 87 1990 7235 7239
6. F.M. Keane, S. Chowdhury, T.-W. Yao, N.A. Nadvi, M.G. Gall, Y. Chen, B. Osborne, A.J. Vieira de Ribeiro, W.B. Church, G.W. McCaughan, M.D. Gorrell, and D.M.T. Yu Targeting dipeptidyl peptidase-4 (DPP-4) and fibroblast activation protein (FAP) for diabetes and cancer therapy B. Dunn, Proteinases as Drug Targets 2012 RSC Cambridge 119 145
7. M.A. Huber, N. Kraut, J.E. Park, R.D. Schubert, W.J. Rettig, R.U. Peter, and P. Garin-Chesa Fibroblast activation protein: differential expression and serine protease activity in reactive stromal fibroblasts of melanocytic skin tumors J. Invest. Dermatol. 120 2003 182 188
8. M.T. Levy, G.W. McCaughan, C.A. Abbott, J.E. Park, A.M. Cunningham, E. Muller, W.J. Rettig, and M.D. Gorrell Fibroblast activation protein: a cell surface dipeptidyl peptidase and gelatinase expressed by stellate cells at the tissue remodelling interface in human cirrhosis Hepatology 29 1999 1768 1778
9. J. Niedermeyer, M. Kriz, F. Hilberg, P. Garin-Chesa, U. Bamberger, M.C. Lenter, J. Park, B. Viertel, H. Puschner, M. Mauz, W.J. Rettig, and A. Schnapp Targeted disruption of mouse fibroblast activation protein Mol. Cell. Biol. 20 2000 1089 1094
10. W.N. Brennen, J.T. Isaacs, and S.R. Denmeade Rationale behind targeting fibroblast activation protein-expressing carcinoma-associated fibroblasts as a novel chemotherapeutic strategy Mol. Cancer Ther. 11 2012 257 266
11. L.-C.S. Wang, A. Lo, J. Scholler, J. Sun, R. Majumdar, V. Kapoor, M. Antzis, C.E. Cotner, L.A. Johnson, A.C. Durham, C. Solomides, C.H. June, E. Pure, and S.M. Albelda Targeting fibroblast activation protein in tumor stroma with chimeric antigen receptor t cells can inhibit tumor growth and augment host immunity without severe toxicity Cancer Immunol. Res. 2 2014 154 166
12. M. Kraman, P.J. Bambrough, J.N. Arnold, E.W. Roberts, L. Magiera, J.O. Jones, A. Gopinathan, D.A. Tuveson, and D.T. Fearon Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-{alpha} Science 330 2010 827 830
13. X.M. Wang, D.M.T. Yu, G.W. McCaughan, and M.D. Gorrell Fibroblast activation protein increases apoptosis, cell adhesion and migration by the LX-2 human stellate cell line Hepatology 42 2005 935 945
14. K. Aertgeerts, I. Levin, L. Shi, G.P. Snell, A. Jennings, G.S. Prasad, Y. Zhang, M.L. Kraus, S. Salakian, V. Sridhar, R. Wijnands, and M.G. Tennant Structural and kinetic analysis of the substrate specificity of human fibroblast activation protein alpha J. Biol. Chem. 280 2005 19441 19444
15. M.D. Gorrell Dipeptidyl peptidase IV and related enzymes in cell biology and liver disorders Clin. Sci. (Lond.) 108 2005 277 292
16. D. Rea, and V. Fülöp Prolyl oligopeptidase structure and dynamics CNS Neurol. Disord. Drug Targets 10 2011 306 310
17. J.E. Park, M.C. Lenter, R.N. Zimmermann, P. Garin-Chesa, L.J. Old, and W.J. Rettig Fibroblast activation protein: a dual-specificity serine protease expressed in reactive human tumor stromal fibroblasts J. Biol. Chem. 274 1999 36505 36512
18. N.L. Thompson, D.C. Hixson, H. Callanan, M. Panzica, D. Flanagan, R.A. Faris, W.J. Hong, S. Hartel-Schenk, and D. Doyle A Fischer rat substrain deficient in dipeptidyl peptidase IV activity makes normal steady-state RNA levels and an altered protein. Use as a liver-cell transplantation model Biochem. J. 273 1991 497 502
19. E. Tsuji, Y. Misumi, T. Fujiwara, N. Takami, S. Ogata, and Y. Ikehara An active-site mutation (Gly633Arg) of dipeptidyl peptidase IV causes its retention and rapid degradation in the endoplasmic reticulum Biochemistry 31 1992 11921 11927
20. C.A. Abbott, G.W. McCaughan, M.T. Levy, W.B. Church, and M.D. Gorrell Binding to human dipeptidyl peptidase IV by adenosine deaminase and antibodies that inhibit ligand binding involves overlapping, discontinuous sites on a predicted beta propeller domain Eur. J. Biochem. 266 1999 798 810
21. C.A. Abbott, G.W. McCaughan, and M.D. Gorrell Two highly conserved glutamic acid residues in the predicted beta propeller domain of dipeptidyl peptidase IV are required for its enzyme activity FEBS Lett. 458 1999 278 284
22. Z. Szeltner, T. Juhasz, I. Szamosi, D. Rea, V. Fülöp, K. Modos, L. Juliano, and L. Polgar The loops facing the active site of prolyl oligopeptidase are crucial components in substrate gating and specificity Biochim. Biophys. Acta 1834 2013 98 111
23. M.L. Pineiro-Sanchez, L.A. Goldstein, J. Dodt, L. Howard, Y. Yeh, and W.T. Chen Identification of the 170-kDa melanoma membrane-bound gelatinase (seprase) as a serine integral membrane protease J. Biol. Chem. 272 1997 7595 7601
24. D. Rea, and V. Fülöp Structure-function properties of prolyl oligopeptidase family enzymes Cell Biochem. Biophys. 44 2006 349 365
25. X.M. Wang, T.-W. Yao, N.A. Nadvi, B. Osborne, G.W. McCaughan, and M.D. Gorrell Fibroblast activation protein and chronic liver disease Front. Biosci. 13 2008 3168 3180
26. J.L. Brodsky Cleaning up: ER-associated degradation to the rescue Cell 151 2012 1163 1167
27. M. Boyce, and J. Yuan Cellular response to endoplasmic reticulum stress: a matter of life or death Cell Death Differ. 13 2006 363 373
28. J. Wu, and R.J. Kaufman From acute ER stress to physiological roles of the unfolded protein response Cell Death Differ. 13 2006 374 384
29. K. Mori Tripartite management of unfolded proteins in the endoplasmic reticulum Cell 101 2000 451 454
30. Y. Li, K. Laue, S. Temtamy, M. Aglan, L.D. Kotan, G. Yigit, H. Canan, B. Pawlik, G. Nürnberg, E.L. Wakeling, O.W. Quarrell, I. Baessmann, M.B. Lanktree, M. Yilmaz, R.A. Hegele, K. Amr, K.W. May, P. Nürnberg, A.K. Topaloglu, M. Hammerschmidt, and B. Wollnik Temtamy preaxial brachydactyly syndrome is caused by loss-of-function mutations in chondroitin synthase 1, a potential target of BMP signaling Am. J. Hum. Genet. 87 2010 757 767
31. I. Carr, K. Flintoff, G. Taylor, A. Markham, and D. Bonthron Interactive visual analysis of SNP data for rapid autozygosity mapping in consanguineous families Hum. Mutat. 27 2006 1041 1046
32. G.W. Lynch, E.K. Slaytor, F.D. Elliott, A. Saurajen, S.G. Turville, A.J. Sloane, P.U. Cameron, A.L. Cunningham, and G.M. Halliday CD4 is expressed by epidermal Langerhans' cells predominantly as covalent dimers Exp. Dermatol. 12 2003 700 711
33. K. Ajami, C.A. Abbott, G.W. McCaughan, and M.D. Gorrell Dipeptidyl peptidase 9 has two forms, a broad tissue distribution, cytoplasmic localization and DPIV-like peptidase activity Biochim. Biophys. Acta Gene Struct. Expr. 1679 2004 18 28
34. D.M.T. Yu, X.M. Wang, G.W. McCaughan, and M.D. Gorrell Extra-enzymatic functions of the dipeptidyl peptidase (DP) IV related proteins DP8 and DP9 in cell adhesion, migration and apoptosis FEBS J. 273 2006 2447 2461
35. S. Chowdhury, Y. Chen, T.-W. Yao, K. Ajami, X.M. Wang, Y. Popov, D. Schuppan, P. Bertolino, G.W. McCaughan, D.M. Yu, and M.D. Gorrell Regulation of dipeptidyl peptidase 8 and 9 expression in activated lymphocytes and injured liver World J. Gastroenterol. 19 2013 2883 2893
36. D.M. Yu, K. Ajami, M.G. Gall, J. Park, C.S. Lee, K.A. Evans, E.A. McLaughlin, M.R. Pitman, C.A. Abbott, G.W. McCaughan, and M.D. Gorrell The in vivo expression of dipeptidyl peptidases 8 and 9 J. Histochem. Cytochem. 57 2009 1025 1040
37. J. Park, H.M. Knott, N.A. Nadvi, C.A. Collyer, X.M. Wang, W.B. Church, and M.D. Gorrell Reversible inactivation of human dipeptidyl peptidases 8 and 9 by oxidation Open Enz. Inhib. J. 1 2008 52 61
38. T.-W. Yao, W.-S. Kim, D.M. Yu, G. Sharbeen, G.W. McCaughan, K.-Y. Choi, P. Xia, and M.D. Gorrell A novel role of dipeptidyl peptidase 9 in epidermal growth factor signaling Mol. Cancer Res. 9 2011 948 959
39. C.A. Abbott, and M.D. Gorrell The family of CD26/DPIV and related ectopeptidases J. Langner, S. Ansorge, Ectopeptidases: CD13/Aminopeptidase N and CD26/Dipeptidylpeptidase IV in Medicine and Biology 2002 Kluwer/Plenum NY 171 195
40. E.S. Lander, and D. Botstein Homozygosity mapping: a way to map human recessive traits with the DNA of inbred children Science 236 1987 1567 1570
41. A. Thielitz, R.W. Vetter, B. Schultze, S. Wrenger, L. Simeoni, S. Ansorge, K. Neubert, J. Faust, P. Lindenlaub, H.P. Gollnick, and D. Reinhold Inhibitors of dipeptidyl peptidase IV-like activity mediate antifibrotic effects in normal and keloid-derived skin fibroblasts J. Invest. Dermatol. 128 2008 855 866
42. E. Fujita, Y. Kouroku, A. Isoai, H. Kumagai, A. Misutani, C. Matsuda, Y.K. Hayashi, and T. Momoi Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II) Hum. Mol. Genet. 16 2007 618 629
43. Y. Ishida, A. Yamamoto, A. Kitamura, S.R. Lamandé, T. Yoshimori, J.F. Bateman, H. Kubota, and K. Nagata Autophagic elimination of misfolded procollagen aggregates in the endoplasmic reticulum as a means of cell protection Mol. Biol. Cell 20 2009 2744 2754
44. K.Y. Tsang, D. Chan, J.F. Bateman, and K.S. Cheah In vivo cellular adaptation to ER stress: survival strategies with double-edged consequences J. Cell Sci. 123 2010 2145 2154
45. S. Wang, and R.J. Kaufman The impact of the unfolded protein response on human disease J. Cell Biol. 197 2012 857 867
46. S. Oyadomari, and M. Mori Roles of CHOP/GADD153 in endoplasmic reticulum stress Cell Death Differ. 11 2003 381 389
47. B. Turk, D. Turk, and V. Turk Protease signalling: the cutting edge EMBO J. 31 2012 1630 1643
48. C.E. Brokopp, R. Schoenauer, P. Richards, S. Bauer, C. Lohmann, M.Y. Emmert, B. Weber, S. Winnik, E. Aikawa, K. Graves, M. Genoni, P. Vogt, T.F. Lüscher, C. Renner, S.P. Hoerstrup, and C.M. Matter Fibroblast activation protein is induced by inflammation and degrades type I collagen in thin-cap fibroatheromata Eur. Heart J. 32 2011 2713 2722
49. M. Jacob, L. Chang, and E. Pure Fibroblast activation protein in remodeling tissues Curr. Mol. Med. 12 2012 1220 1243
50. V.J. Christiansen, K.W. Jackson, K.N. Lee, T.D. Downs, and P.A. McKee Targeting inhibition of fibroblast activation protein-α and prolyl oligopeptidase activities on cells common to metastatic tumor microenvironments Neoplasia 15 2013 348 358
51. H.B. Rasmussen, S. Branner, F.C. Wiberg, and N. Wagtmann Crystal structure of human DPP-IV/CD26 in complex with a substrate analogue Nat. Struct. Biol. 10 2003 19 25
52. A. Vitale, and R.S. Boston Endoplasmic Reticulum quality control and the unfolded protein response: insights from plants Traffic 9 2008 1581 1588
53. M. Ogata, S.-I. Hino, A. Saito, K. Morikawa, S. Kondo, S. Kanemoto, T. Murakami, M. Taniguchi, I. Tanii, K. Yoshinaga, S. Shiosaka, J.A. Hammarback, F. Urano, and K. Imaizumi Autophagy is activated for cell survival after endoplasmic reticulum stress Mol. Cell. Biol. 6 2006 9220 9231
54. Y. Kozutsumi, M. Segal, K. Normington, M.J. Gething, and J. Sambrook The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins Nature 332 1988 462 464
55. D. Dong, M. Ni, J. Li, S. Xiong, W. Ye, J.J. Virrey, C. Mao, R. Ye, M. Wang, L. Pen, L. Dubeau, S. Groshen, F.M. Hofman, and A.S. Lee Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development Cancer Res. 68 2008 498 505
56. R.R. Kopito ER quality control: the cytoplasmic connection Cell 88 1997 427 430
57. A.H. Schönthal Endoplasmic reticulum stress and autophagy as targets for cancer therapy Cancer Lett. 275 2009 163 169
58. X.Z. Wang, B. Lawson, J.W. Brewer, H. Zinszner, A. Sanjay, L.J. Mi, R. Boorstein, G. Kreibich, L.M. Hendershot, and D. Ron Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153) Mol. Cell. Biol. 16 1996 4273 4280
59. J.W. Brewer, and J.A. Diehl PERK mediates cell-cycle exit during the mammalian unfolded protein response Proc. Natl. Acad. Sci. U. S. A. 97 2000 12625 12630
60. J. Niedermeyer, P. Garin-Chesa, M. Kriz, F. Hilberg, E. Mueller, U. Bamberger, W.J. Rettig, and A. Schnapp Expression of the fibroblast activation protein during mouse embryo development Int. J. Dev. Biol. 45 2001 445 447
61. F.M. Keane, T.-W. Yao, S. Seelk, M.G. Gall, S. Chowdhury, S.E. Poplawski, J.H. Lai, Y. Li, W. Wu, P. Farrell, A.J. Vieira de Ribeiro, B. Osborne, D.M.T. Yu, D. Seth, K. Rahman, P. Haber, A.K. Topaloglu, C. Wang, S. Thomson, A. Hennessy, J. Prins, S.M. Twigg, S.V. McLennan, G.W. McCaughan, W.W. Bachovchin, and M.D. Gorrell Quantitation of fibroblast activation protein (FAP)-specific protease activity in mouse, baboon and human fluids and organs FEBS Open Biol. 4 2014 43 54
62. X.M. Wang, S. Cordoba, D. Marguet, W. Rettig, A. Schnapp, G.W. McCaughan, and M.D. Gorrell Reduced hepatic fibrosis is associated with fewer intrahepatic B cells in fibroblast activation protein and dipeptidyl peptidase IV gene knockout mice Hepatology 46 2007 299A
63. C.A. Abbott, D. Koorey, and G.W. McCaughan An EcoRI polymorphism within the dipeptidyl peptidase IV (DPPIV) gene Hum. Mol. Genet. 2 1993 1507
64. T. Fujiwara, E. Tsuji, Y. Misumi, N. Takami, and Y. Ikehara Selective cell-surface expression of dipeptidyl peptidase IV with mutations at the active site sequence Biochem. Biophys. Res. Commun. 185 1992 776 784