Mast cell tryptase stimulates production of decorin by human testicular peritubular cells: Possible role of decorin in male infertility by interfering with growth factor signaling

Human Reproduction

Volumn 26, Issue 10, 2011, Pages 2613-2625

  Adam, M ^a   Schwarzer, J U ^b   Khn, F M ^c   Strauss, L ^d   Poutanen, M ^d   Mayerhofer, A ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b Praxis Urology Andrology   (Germany)

^c Andrologicum   (Germany)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

decorin; fibrosis; paracrine; proliferation; Testis

Indexed keywords

CALCIUM ION; CALPONIN; COLLAGEN TYPE 4; DECORIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; MESSENGER RNA; MYOSIN HEAVY CHAIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SCATTER FACTOR RECEPTOR; SMOOTH MUSCLE ACTIN; SOMATOMEDIN C RECEPTOR; THY 1 ANTIGEN; TRYPTASE; VASCULOTROPIN RECEPTOR;

ARTICLE; CALCIUM CELL LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FIBROSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MALE INFERTILITY; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TESTIS ATROPHY; TESTIS BIOPSY; TESTIS CELL; TESTIS FIBROSIS; TESTIS PERITUBULAR CELL; WESTERN BLOTTING;

EID: 80052872193     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/der245     Document Type: Article

References (59)

1. Albrecht M, Frungieri MB, Kunz L, Ramsch R, Meineke V, Kohn FM, Mayerhofer A. Divergent effects of the major mast cell products histamine, tryptase and TNF-alpha on human fibroblast behaviour. Cell Mol Life Sci 2005;62:2867-2876. (Pubitemid 41779952)
2. Albrecht M, Ramsch R, Kohn FM, Schwarzer JU, Mayerhofer A. Isolation and cultivation of human testicular peritubular cells: a new model for the investigation of fibrotic processes in the human testis and male infertility. J Clin Endocrinol Metab 2006;91:1956-1960.
3. Basciani S, Mariani S, Arizzi M, Ulisse S, Rucci N, Jannini EA, Della Rocca C, Manicone A, Carani C, Spera G et al. Expression of platelet-derived growth factor-A (PDGF-A), PDGF-B, and PDGF receptor-alpha and-beta during human testicular development and disease. J Clin Endocrinol Metab 2002;87:2310-2319. (Pubitemid 34521525)
4. Basciani S, Mariani S, Spera G, Gnessi L. Role of platelet-derived growth factors in the testis. Endocr Rev 2010;31:916-939.
5. Cigorraga SB, Chemes H, Pellizzari E. Steroidogenic and morphogenic characteristics of human peritubular cells in culture. Biol Reprod 1994; 51:1193-1205. (Pubitemid 24354279)
6. Csordas G, Santra M, Reed CC, Eichstetter I, McQuillan DJ, Gross D, Nugent MA, Hajnoczky G, Iozzo RV. Sustained down-regulation of the epidermal growth factor receptor by decorin. A mechanism for controlling tumor growth in vivo. J Biol Chem 2000;275:32879-32887.
7. D'Antoni ML, Torregiani C, Ferraro P, Michoud MC, Mazer B, Martin JG, Ludwig MS. Effects of decorin and biglycan on human airway smooth muscle cell proliferation and apoptosis. Am J Physiol Lung Cell Mol Physiol 2008;294:L764-L771. (Pubitemid 351520110)
8. Davidoff MS, Breucker H, Holstein AF, Seidl K. Cellular architecture of the lamina propria of human seminiferous tubules. Cell Tissue Res 1990; 262:253-261. (Pubitemid 20344865)
9. De Kretser D, Baker H. Human infertility: the male factor. In: Adashi EY, Rock JA, Rosenwaks Z (eds) Reproductive endocrinology, surgery and technology. Philadelphia: Lippincott-Raven, 1996,2031-2062.
10. Dobashi M, Fujisawa M, Naito I, Yamazaki T, Okada H, Kamidono S. Distribution of type IV collagen subtypes in human testes and their association with spermatogenesis. Fertil Steril 2003;80 Suppl 2:755-760. (Pubitemid 37152390)
11. Dreux AC, Lamb DJ, Modjtahedi H, Ferns GA. The epidermal growth factor receptors and their family of ligands: their putative role in atherogenesis. Atherosclerosis 2006;186:38-53.
12. Fadic R, Mezzano V, Alvarez K, Cabrera D, Holmgren J, Brandan E. Increase in decorin and biglycan in Duchenne Muscular Dystrophy: role of fibroblasts as cell source of these proteoglycans in the disease. J Cell Mol Med 2006;10:758-769. (Pubitemid 44874284)
13. Ferdous Z, Peterson SB, Tseng H, Anderson DK, Iozzo RV, Grande-Allen KJ. A role for decorin in controlling proliferation, adhesion, and migration of murine embryonic fibroblasts. J Biomed Mater Res A 2010;93:419-428.
14. Fohr KJ, Mayerhofer A, Sterzik K, Rudolf M, Rosenbusch B, Gratzl M. Concerted action of human chorionic gonadotropin and norepinephrine on intracellular-free calcium in human granulosa-lutein cells: evidence for the presence of a functional alpha-adrenergic receptor. J Clin Endocrinol Metab 1993;76:367-373. (Pubitemid 23073057)
15. Frungieri MB, Calandra RS, Lustig L, Meineke V, Kohn FM, Vogt HJ, Mayerhofer A. Number, distribution pattern, and identification of macrophages in the testes of infertile men. Fertil Steril 2002a;78:298-306. (Pubitemid 34831730)
16. Frungieri MB, Weidinger S, Meineke V, Kohn FM, Mayerhofer A. Proliferative action of mast-cell tryptase is mediated by PAR2, COX-2, prostaglandins, and PPAR. PNAS 2002b;99:15072-15077.
17. Gambichler T, Kreuter A, Skrygan M, Burkert B, Altmeyer P, Schieren G. Decorin is significantly overexpressed in nephrogenic systemic fibrosis. Am J Clin Pathol 2009;132:139-143.
18. Gnessi L, Emidi A, Jannini EA, Carosa E, Maroder M, Arizzi M, Ulisse S, Spera G. Testicular development involves the spatiotemporal control of PDGFs and PDGF receptors gene expression and action. J Cell Biol 1995;131:1105-1121.
19. Goldoni S, Humphries A, Nystrom A, Sattar S, Owens RT, McQuillan DJ, Ireton K, Iozzo RV. Decorin is a novel antagonistic ligand of the Met receptor. J Cell Biol 2009;185:743-754.
20. Gulkesen KH, Erdogru T, Sargin CF, Karpuzoglu G. Expression of extracellular matrix proteins and vimentin in testes of azoospermic man: an immunohistochemical and morphometric study. Asian J Androl 2002;4:55-60. (Pubitemid 34269634)
21. Haider SG, Talati J, Servos G. Ultrastructure of peritubular tissue in association with tubular hyalinization in human testis. Tissue Cell 1999; 31:90-98. (Pubitemid 29201977)
22. Iacob D, Cai J, Tsonis M, Babwah A, Chakraborty C, Bhattacharjee RN, Lala PK. Decorin-mediated inhibition of proliferation and migration of the human trophoblast via different tyrosine kinase receptors. Endocrinology 2008;149:6187-6197.
23. Iozzo RV, Schaefer L. Proteoglycans in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J 2010;277:3864-3875.
24. Ivey ME, Little PJ. Thrombin regulates vascular smooth muscle cell proteoglycan synthesis via PAR-1 and multiple downstream signalling pathways. Thromb Res 2008;123:288-297.
25. Kozma EM, Wisowski G, Olczyk K. Platelet derived growth factor BB is a ligand for dermatan sulfate chain(s) of small matrix proteoglycans from normal and fibrosis affected fascia. Biochimie 2009;91:1394-1404.
26. Kunz L, Ramsch R, Krieger A, Young KA, Dissen GA, Stouffer RL, Ojeda SR, Mayerhofer A. Voltage-dependent K+ channel acts as sex steroid sensor in endocrine cells of the human ovary. J Cell Physiol 2006;206:167-174. (Pubitemid 41740728)
27. Li X, Strauss L, Kaatrasalo A, Mayerhofer A, Huhtaniemi I, Santti R, Makela S, Poutanen M. Transgenic mice expressing p450 aromatase as a model for male infertility associated with chronic inflammation in the testis. Endocrinology 2006;147:1271-1277. (Pubitemid 43244360)
28. Macri L, Silverstein D, Clark RA. Growth factor binding to the pericellular matrix and its importance in tissue engineering. Adv Drug Deliv Rev 2007; 59:1366-1381. (Pubitemid 350090013)
29. Maekawa M, Kamimura K, Nagano T. Peritubular myoid cells in the testis: their structure and function. Arch Histol Cytol 1996;59:1-13.
30. Mariani S, Basciani S, Arizzi M, Spera G, Gnessi L. PDGF and the testis. Trends Endocrinol Metab 2002;13:11-17. (Pubitemid 36734010)
31. Matzkin ME, Mayerhofer A, Rossi SP, Gonzalez B, Gonzalez CR, Gonzalez-Calvar SI, Terradas C, Ponzio R, Puigdomenech E, Levalle O et al. Cyclooxygenase-2 in testes of infertile men: evidence for the induction of prostaglandin synthesis by interleukin-1beta. Fertil Steril 2010;94:1933-1936.
32. Mauviel A, Santra M, Chen YQ, Uitto J, Iozzo RV. Transcriptional regulation of decorin gene expression. Induction by quiescence and repression by tumor necrosis factor-alpha. J Biol Chem 1995; 270:11692-11700.
33. Meineke V, Frungieri MB, Jessberger B, Vogt H, Mayerhofer A. Human testicular mast cells contain tryptase: increased mast cell number and altered distribution in the testes of infertile men. Fertil Steril 2000; 74:239-244. (Pubitemid 30604184)
34. Miqueloto CA, Zorn TM. Characterization and distribution of hyaluronan and the proteoglycans decorin, biglycan and perlecan in the developing embryonic mouse gonad. J Anat 2007;211:16-25. (Pubitemid 47034507)
35. Nakazumi H, Sasano H, Maehara I, Orikasa S. Transforming growth factor-alpha, epidermal growth factor, and epidermal growth factor receptor in human testis obtained from biopsy and castration: immunohistochemical study. Tohoku J Exp Med 1996;178:381-388. (Pubitemid 126501728)
36. Nili N, Cheema AN, Giordano FJ, Barolet AW, Babaei S, Hickey R, Eskandarian MR, Smeets M, Butany J, Pasterkamp G et al. Decorin inhibition of PDGF-stimulated vascular smooth muscle cell function: potential mechanism for inhibition of intimal hyperplasia after balloon angioplasty. Am J Pathol 2003;163:869-878. (Pubitemid 37040123)
37. Nurmio M, Toppari J, Zaman F, Andersson AM, Paranko J, Soder O, Jahnukainen K. Inhibition of tyrosine kinases PDGFR and C-Kit by imatinib mesylate interferes with postnatal testicular development in the rat. Int J Androl 2007;30:366-376. (Pubitemid 47254397)
38. Puglianiello A, Campagnolo L, Farini D, Cipollone D, Russo MA, Siracusa G. Expression and role of PDGF-BB and PDGFR-beta during testis morphogenesis in the mouse embryo. J Cell Sci 2004; 117:1151-1160. (Pubitemid 38456096)
39. Pulkkinen L, Alitalo T, Krusius T, Peltonen L. Expression of decorin in human tissue and cell lines and chromosomal assignment of the gene locus (DCN). Cytogenet Cell Genet 1992;60:107-111.
40. Reed CC, Iozzo RV. The role of decorin in collagen fibrillogenesis and skin homeostasis. Glycoconj J 2002;19:249-255. (Pubitemid 37174552)
41. Ricci G, Catizone A, Galdieri M. Embryonic mouse testis development: role of platelet derived growth factor (PDGF-BB). J Cell Physiol 2004; 200:458-467. (Pubitemid 39006938)
42. Romano F, Tripiciano A, Muciaccia B, De Cesaris P, Ziparo E, Palombi F, Filippini A. The contractile phenotype of peritubular smooth muscle cells is locally controlled: possible implications in male fertility. Contraception 2005;72:294-297. (Pubitemid 41338111)
43. Romano F, Chiarenza C, Palombi F, Filippini A, Padula F, Ziparo E, De Cesaris P. Platelet-derived growth factor-BB-induced hypertrophy of peritubular smooth muscle cells is mediated by activation of p38 MAP-kinase and of Rho-kinase. J Cell Physiol 2006;207:123-131.
44. Rossi F, Ferraresi A, Romagni P, Silvestroni L, Santiemma V. Angiotensin II stimulates contraction and growth of testicular peritubular myoid cells in vitro. Endocrinology 2002;143:3096-3104. (Pubitemid 34809882)
45. Saito Y, Haendeler J, Hojo Y, Yamamoto K, Berk BC. Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol Cell Biol 2001;21:6387-6394. (Pubitemid 32927407)
46. Santoro G, Romeo C, Impellizzeri P, Gentile C, Anastasi G, Santoro A. Ultrastructural and immunohistochemical study of basal lamina of the testis in adolescent varicocele. Fertil Steril 2000;73:699-705. (Pubitemid 30154106)
47. Schaefer L, Iozzo RV. Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J Biol Chem 2008; 283:21305-21309.
48. Schell C, Albrecht M, Mayer C, Schwarzer JU, Frungieri MB, Mayerhofer A. Exploring human testicular peritubular cells: identification of secretory products and regulation by tumor necrosis factor-alpha. Endocrinology 2008;149:1678-1686. (Pubitemid 351468356)
49. Schell C, Albrecht M, Spillner S, Mayer C, Kunz L, Köhn FM, Schwarzer U, Mayerhofer A. 15-deoxy-delta-Prostaglandin-J2 (15dPGJ2) induces hypertrophy and loss of contractility in human testicular peritubular cells: Implications for human male fertility. Endocrinology 2010; 151:1257-1268.
50. Seidler DG, Dreier R. Decorin and its galactosaminoglycan chain: extracellular regulator of cellular function? IUBMB Life 2008;60: 729-733.
51. Spiess AN, Feig C, Schulze W, Chalmel F, Cappallo-Obermann H, Primig M, Kirchhoff C. Cross-platform gene expression signature of human spermatogenic failure reveals inflammatory-like response. Hum Reprod 2007;22:2936-2946. (Pubitemid 351696823)
52. Spinnler K, Kohn FM, Schwarzer U, Mayerhofer A. Glial cell line-derived neurotrophic factor is constitutively produced by human testicular peritubular cells and may contribute to the spermatogonial stem cell niche in man. Hum Reprod 2010;25:2181-2187.
53. Strauss L, Kallio J, Desai N, Pakarinen P, Miettinen T, Gylling H, Albrecht M, Makela S, Mayerhofer A, Poutanen M. Increased exposure to estrogens disturbs maturation, steroidogenesis, and cholesterol homeostasis via estrogen receptor alpha in adult mouse Leydig cells. Endocrinology 2009;150:2865-2872.
54. Ungefroren H, Ergun S, Krull NB, Holstein AF. Expression of the small proteoglycans biglycan and decorin in the adult human testis. Biol Reprod 1995;52:1095-1105.
55. Van Straaten JF, Coers W, Noordhoek JA, Huitema S, Flipsen JT, Kauffman HF, Timens W, Postma DS. Proteoglycan changes in the extracellular matrix of lung tissue from patients with pulmonary emphysema. Mod Pathol 1999;12:697-705. (Pubitemid 29354883)
56. Wegrowski Y, Paltot V, Gillery P, Kalis B, Randoux A, Maquart FX. Stimulation of sulphated glycosaminoglycan and decorin production in adult dermal fibroblasts by recombinant human interleukin-4. Biochem J 1995;307:673-678.
57. Welsh M, Saunders PT, Atanassova N, Sharpe RM, Smith LB. Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB J 2009;23:4218-4230.
58. Zhang C, Yeh S, Chen YT, Wu CC, Chuang KH, Lin HY, Wang RS, Chang YJ, Mendis-Handagama C, Hu L et al. Oligozoospermia with normal fertility in male mice lacking the androgen receptor in testis peritubular myoid cells. Proc Natl Acad Sci USA 2006;103:17718-17723. (Pubitemid 44852226)
59. Zhu JX, Goldoni S, Bix G, Owens RT, McQuillan DJ, Reed CC, Iozzo RV. Decorin evokes protracted internalization and degradation of the epidermal growth factor receptor via caveolar endocytosis. J Biol Chem 2005;280:32468-32479. (Pubitemid 41361859)