Transglutaminase 4 as a prostate autoantigen in male subfertility

Science Translational Medicine

Volumn 7, Issue 292, 2015, Pages

  Landegren, Nils ^a,b   Sharon, Donald ^c,d   Shum, Anthony K ^e   Khan, Imran S ^f   Fasano, Kayla J ^f   Hallgren, Åsa ^a,b   Kampf, Caroline ^b   Freyhult, Eva ^b   Ardesjö Lundgren, Brita ^g   Alimohammadi, Mohammad ^a,b   Rathsman, Sandra ^h   Ludvigsson, Jonas F ⁱ   Lundh, Dan ^j   Motrich, Ruben ^k   Rivero, Virginia ^k   Fong, Lawrence ^l   Giwercman, Aleksander ^m   Gustafsson, Jan ^b   Perheentupa, Jaakko ⁿ   Husebye, Eystein S ^o   Anderson, Mark S ^f   Snyder, Michael ^c   Kämpe, Olle ^a,b   more..

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c STANFORD UNIVERSITY   (United States)

^d YALE UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^h ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

ⁱ KAROLINSKA INSTITUTE   (Sweden)

^j UNIVERSITY OF SKÖVDE   (Sweden)

^k UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^l UNIVERSITY OF CALIFORNIA   (United States)

^m LUND UNIVERSITY   (Sweden)

ⁿ UNIVERSITY OF HELSINKI   (Finland)

^o UNIVERSITY OF BERGEN   (Norway)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; PROSTATE ANTIGEN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEOME; TRANSGLUTAMINASE 4; UNCLASSIFIED DRUG; AUTOANTIGEN; AUTOIMMUNE REGULATOR PROTEIN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE POLYENDOCRINOPATHY CANDIDIASIS ECTODERMAL DYSTROPHY; AUTOIMMUNITY; BLOOD SAMPLING; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME RELEASE; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; LIGAND BINDING; MAJOR CLINICAL STUDY; MALE; MALE SUBFERTILITY; MOUSE; NONHUMAN; PHYLOGENETIC TREE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSTATITIS; PROTEIN EXPRESSION; REPRODUCTION; SCREENING; SUBFERTILITY; THYMUS; TISSUE MICROARRAY; ANIMAL; C57BL MOUSE; DEFICIENCY; ENZYMOLOGY; IMMUNOLOGY; MALE INFERTILITY; METABOLISM; PATHOLOGY; POLYENDOCRINOPATHY; PROSTATE; PROTEOMICS; PUBERTY;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; EPITHELIAL CELLS; FEMALE; HUMANS; INFERTILITY, MALE; MALE; MICE, INBRED C57BL; POLYENDOCRINOPATHIES, AUTOIMMUNE; PROSTATE; PROSTATITIS; PROTEOME; PROTEOMICS; PUBERTY; THYMUS GLAND; TRANSCRIPTION FACTORS; TRANSGLUTAMINASES;

EID: 84931466170     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaa9186     Document Type: Article

References (50)

1. C. Krausz, Male infertility: Pathogenesis and clinical diagnosis. Best Pract. Res. Clin. Endocrinol. Metab. 25, 271-285 (2011).
2. B. D. Anawalt, Approach to male infertility and induction of spermatogenesis. J. Clin. Endocrinol. Metab. 98, 3532-3542 (2013).
3. P. J. Stahl, D. S. Stember, M. Goldstein, Contemporary management of male infertility. Annu. Rev. Med. 63, 525-540 (2012).
4. S. Alshahrani, J. McGill, A. Agarwal, Prostatitis and male infertility. J. Reprod. Immunol. 100, 30-36 (2013).
5. M. Fraczek, M. Kurpisz, Inflammatory mediators exert toxic effects of oxidative stress on human spermatozoa. J. Androl. 28, 325-333 (2007).
6. M. Marconi, A. Pilatz, F. Wagenlehner, T. Diemer, W. Weidner, Impact of infection on the secretory capacity of the male accessory glands. Int. Braz. J. Urol. 35, 299-309 (2009).
7. R. D. Motrich, J. P. Mackern-Oberti, M. Maccioni, V. E. Rivero, Effects of autoimmunity to the prostate on the fertility of the male rat. Fertil. Steril. 91, 2273-2280 (2009).
8. T. Kullisaar, S. Türk, M. Punab, R. Mändar, Oxidative stress - Cause or consequence of male genital tract disorders? Prostate 72, 977-983 (2012).
9. P. Ahonen, S. Myllärniemi, I. Sipilä, J. Perheentupa, Clinical variation of autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) in a series of 68 patients. N. Engl. J. Med. 322, 1829-1836 (1990).
10. M. S. Anderson, E. S. Venanzi, L. Klein, Z. Chen, S. P. Berzins, S. J. Turley, H. von Boehmer, R. Bronson, A. Dierich, C. Benoist, D. Mathis, Projection of an immunological self shadow within the thymus by the aire protein. Science 298,1395-1401 (2002).
11. M. H. Cheng, M. S. Anderson, Monogenic autoimmunity. Annu. Rev. Immunol. 30, 393-427 (2012).
12. M. Alimohammadi, N. Dubois, F. Sköldberg, Å. Hallgren, I. Tardivel, H. Hedstrand, J. Haavik, E. S. Husebye, J. Gustafsson, F. Rorsman, A. Meloni, C. Janson, B. Vialettes, M. Kajosaari, W. Egner, R. Sargur, F. Pontén, Z. Amoura, A. Grimfeld, F. De Luca, C. Betterle, J. Perheentupa, O. Kämpe, J.-C. Carel, Pulmonary autoimmunity as a feature of autoimmune polyendocrine syndrome type 1 and identification of KCNRG as a bronchial autoantigen. Proc. Natl. Acad. Sci. U.S.A. 106, 4396-4401 (2009).
13. J. Perheentupa, APS-I/APECED: The clinical disease and therapy. Endocrinol. Metab. Clin. North Am. 31, 295-320, (2002).
14. C. Ramsey, O. Winqvist, L. Puhakka, M. Halonen, A. Moro, O. Kämpe, P. Eskelin, M. Pelto-Huikko, L. Peltonen, Aire deficient mice develop multiple features of APECED phenotype and show altered immune response. Hum. Mol. Genet. 11,397-409 (2002).
15. F.-X. Hubert, S. A. Kinkel, P. E. Crewther, P. Z. Cannon, K. E. Webster, M. Link, R. Uibo, M. K. O'Bryan, A. Meager, S. P. Forehan, G. K. Smyth, L. Mittaz, S. E. Antonarakis, P. Peterson, W. R. Heath, H. S. Scott, Aire-deficient C57BL/6 mice mimicking the common human 13-base pair deletion mutation present with only a mild autoimmune phenotype. J. Immunol. 182, 3902-3918 (2009).
16. E. Kekäläinen, N. Pöntynen, S. Meri, T. P. Arstila, H. Jarva, Autoimmunity, not a developmental defect, is the cause for subfertility of autoimmune regulator (Aire) deficient mice. Scand. J. Immunol. 81, 298-304 (2015).
17. + regulatory T cells. Blood 107, 1056-1062 (2006).
18. Q.-G. Ruan, K. Tung, D. Eisenman, Y. Setiady, S. Eckenrode, B. Yi, S. Purohit, W.-P. Zheng, Y. Zhang, L. Peltonen, J.-X. She, The autoimmune regulator directly controls the expression of genes critical for thymic epithelial function. J. Immunol. 178,7173-7180 (2007).
19. Y. Hou, J. DeVoss, V. Dao, S. Kwek, J. P. Simko, D. G. McNeel, M. S. Anderson, L. Fong, An aberrant prostate antigen-specific immune response causes prostatitis in mice and is associated with chronic prostatitis in humans. J. Clin. Invest. 119,2031-2041 (2009).
20. H. J. Dubbink, L. de Waal, R. van Haperen, N. S. Verkaik, J. Trapman, J. C. Romijn, The human prostate-specific transglutaminase gene (TGM4): Genomic organization, tissue-specific expression, and promoter characterization. Genomics 51,434-444 (1998).
21. H. J. Dubbink, N. S. Verkaik, P. W. Faber, J. Trapman, F. H. Schröder, J. C. Romijn, Tissue-specific and androgen-regulated expression of human prostate-specific transglutaminase. Biochem. J. 315, 901-908 (1996).
22. M. D. Dean, Genetic disruption of the copulatory plug in mice leads to severely reduced fertility. PLOS Genet. 9, e1003185 (2013).
23. D. C. Mukherjee, A. K. Agrawal, R. Manjunath, A. B. Mukherjee, Suppression of epididymal sperm antigenicity in the rabbit by uteroglobin and transglutaminase in vitro. Science 219, 989-991 (1983).
24. G. Paonessa, S. Metafora, G. Tajana, P. Abrescia, A. De Santis, V. Gentile, R. Porta, Transglutaminase-mediated modifications of the rat sperm surface in vitro. Science 226,852-855 (1984).
25. R. Porta, C. Esposito, A. De Santis, A. Fusco, M. Iannone, S. Metafora, Sperm maturation in human semen: Role of transglutaminase-mediated reactions. Biol. Reprod. 35,965-970 (1986).
26. G. Peluso, R. Porta, C. Esposito, M. A. Tufano, R. Toraldo, M. L. Vuotto, G. Ravagnan, S. Metafora, Suppression of rat epididymal sperm immunogenicity by a seminal vesicle secretory protein and transglutaminase both in vivo and in vitro. Biol. Reprod. 50, 593-602 (1994).
27. W. Dieterich, T. Ehnis, M. Bauer, P. Donner, U. Volta, E. O. Riecken, D. Schuppan, Identification of tissue transglutaminase as the autoantigen of celiac disease. Nat. Med. 3, 797-801 (1997).
28. M. Sárdy, S. Kárpáti, B. Merkl, M. Paulsson, N. Smyth, Epidermal transglutaminase (TGase 3) is the autoantigen of dermatitis herpetiformis. J. Exp. Med. 195, 747-757 (2002).
29. M. Hadjivassiliou, P. Aeschlimann, A. Strigun, D. S. Sanders, N. Woodroofe, D. Aeschlimann, Autoantibodies in gluten ataxia recognize a novel neuronal transglutaminase. Ann. Neurol. 64, 332-343 (2008).
30. M. Franchini, F. Frattini, S. Crestani, C. Bonfanti, Acquired FXIII inhibitors: A systematic review. J. Thromb. Thrombolysis 36, 109-114 (2013).
31. J. L. Thielen, K. G. Volzing, L. S. Collier, L. E. Green, D. A. Largaespada, P. C. Marker, Markers of prostate region-specific epithelial identity define anatomical locations in the mouse prostate that are molecularly similar to human prostate cancers. Differentiation 75, 49-61 (2007).
32. K.-C. Ho, V. E. Quarmby, F. S. French, E. M. Wilson, Molecular cloning of rat prostate transglutaminase complementary DNA. The major androgen-regulated protein DP1 of rat dorsal prostate and coagulating gland. J. Biol. Chem. 267, 12660-12667 (1992).
33. D. A. Goldfarb, B. S. Stein, M. Shamszadeh, R. O. Petersen, Age-related changes in tissue levels of prostatic acid phosphatase and prostate specific antigen. J. Urol. 136, 1266-1269 (1986).
34. J.G.Vieira,S.K.Nishida,A.B.Pereira,R.F.Arraes,I.T.Verreschi,Serumlevelsofprostate-specific antigen in normal boys throughout puberty. J. Clin. Endocrinol. Metab. 78, 1185-1187 (1994).
35. C. Pritchard, B. Mecham, R. Dumpit, I. Coleman, M. Bhattacharjee, Q. Chen, R. A. Sikes, P. S. Nelson, Conserved gene expression programs integrate mammalian prostate development and tumorigenesis. Cancer Res. 69, 1739-1747 (2009).
36. G. Penna, S. Amuchastegui, C. Cossetti, F. Aquilano, R. Mariani, N. Giarratana, E. De Carli, B. Fibbi, L. Adorini, Spontaneous and prostatic steroid binding protein peptide-induced autoimmune prostatitis in the nonobese diabetic mouse. J. Immunol. 179, 1559-1567 (2007).
37. J. J. Devoss, A. K. Shum, K. P. Johannes, W. Lu, A. K. Krawisz, P. Wang, T. Yang, N. P. Leclair, C. Austin, E. C. Strauss, M. S. Anderson, Effector mechanisms of the autoimmune syndrome in the murine model of autoimmune polyglandular syndrome type 1. J. Immunol. 181, 4072-4079 (2008).
38. O. Winqvist, J. Gustafsson, F. Rorsman, F. A. Karlsson, O. Kämpe, Two different cytochrome P450 enzymes are the adrenal antigens in autoimmune polyendocrine syndrome type I and Addison's disease. J. Clin. Invest. 92, 2377-2385 (1993).
39. A. Tsatsoulis, S. M. Shalet, Antisperm antibodies in the polyglandular autoimmune (PGA) syndrome type I: Response to cyclical steroid therapy. Clin. Endocrinol. 35, 299-303 (1991).
40. A. Peter, H. Lilja, Å Lundwall, J. Malm, Semenogelin I and semenogelin II, the major gelforming proteins in human semen, are substrates for transglutaminase. Eur. J. Biochem. 252, 216-221 (1998).
41. S. E. Iismaa, B. M. Mearns, L. Lorand, R. M. Graham, Transglutaminases and disease: Lessons from genetically engineered mouse models and inherited disorders. Physiol. Rev. 89, 991-1023 (2009).
42. L. Lorand, R. M. Graham, Transglutaminases: Crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4, 140-156 (2003).
43. R. Nissinen, L. Paimela, H. Julkunen, P. J. Tienari, M. Leirisalo-Repo, T. Palosuo, O. Vaarala, Peptidylarginine deiminase, the arginine to citrulline converting enzyme, is frequently recognized by sera of patients with rheumatoid arthritis, systemic lupus erythematosus and primary Sjögren syndrome. Scand. J. Rheumatol. 32, 337-342 (2003).
44. F. C. Santos, R. P. Leite, A. M. Custódio, K. P. Carvalho, L. H. Monteiro-Leal, A. B. Santos, R. M. Góes, H. F. Carvalho, S. R. Taboga, Testosterone stimulates growth and secretory activity of the female prostate in the adult gerbil (Meriones unguiculatus). Biol. Reprod. 75, 370-379 (2006).
45. C. V. Obiezu, E. J. Giltay, A. Magklara, A. Scorilas, L. J. Gooren, H. Yu, D. J. Howarth, E. P. Diamandis, Serum and urinary prostate-specific antigen and urinary human glandular kallikrein concentrations are significantly increased after testosterone administration in female-to-male transsexuals. Clin. Chem. 46, 859-862 (2000).
46. R. D. Motrich, M. Maccioni, R. Molina, A. Tissera, J. Olmedo, C. M. Riera, V. E. Rivero, Presence of INFγ-secreting lymphocytes specific to prostate antigens in a group of chronic prostatitis patients. Clin. Immunol. 116, 149-157 (2005).
47. D. Lundh, H. Hedelin, K. Jonsson, M. Gifford, D. Larsson, Assessing chronic pelvic pain syndrome patients: Blood plasma factors and cortisol saliva. Scand. J. Urol. 47, 521-528 (2013).
48. L. E. Murphy, J. L. Mills, A. M. Molloy, C. Qian, T. C. Carter, H. Strevens, D. Wide-Swensson, A. Giwercman, R. J. Levine, Folate and vitamin B12 in idiopathic male infertility. Asian J. Androl. 13, 856-861 (2011).
49. C. Kampf, I. Olsson, U. Ryberg, E. Sjöstedt, F. Pontén, Production of tissue microarrays, immunohistochemistry staining and digitalization within the human protein atlas. J. Vis. Exp. 63, e3620 (2012).
50. T. C. Metzger, I. S. Khan, J. M. Gardner, M. L. Mouchess, K. P. Johannes, A. K. Krawisz, K. M. Skrzypczynska, M. S. Anderson, Lineage tracing and cell ablation identify a post-Aire-expressing thymic epithelial cell population. Cell Rep. 5, 166-179 (2013).