Cytokine expression pattern in benign prostatic hyperplasia infiltrating T cells and impact of lymphocytic infiltration on cytokine mRNA profile in prostatic tissue

Laboratory Investigation

Volumn 83, Issue 8, 2003, Pages 1131-1146

  Steiner, Georg E ^a,c   Stix, Ursula ^a   Handisurya, Alessandra ^a   Willheim, Martin ^a   Haitel, Andrea ^a   Reithmayr, Franz ^a   Paikl, Doris ^a   Ecker, Rupert C ^a   Hrachowitz, Kristian ^a   Kramer, Gero ^a   Lee, Chung ^b   Marberger, Michael ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; CYTOKINE ANTIBODY; CYTOKINE RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; LYMPHOKINE; LYMPHOTOXIN; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CELL ACTIVITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; FLOW CYTOMETRY; HELPER CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOHISTOLOGY; LYMPHOCYTIC INFILTRATION; MALE; PRIORITY JOURNAL; PROSTATE HYPERTROPHY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; TH0 CELL; TH1 CELL; TH2 CELL;

ADULT; CELLS, CULTURED; CYTOKINES; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; IMMUNOENZYME TECHNIQUES; LYMPHOCYTE ACTIVATION; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; PROSTATE; PROSTATIC HYPERPLASIA; RECEPTORS, CYTOKINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TH1 CELLS; TH2 CELLS;

EID: 0042178346     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.LAB.0000081388.40145.65     Document Type: Article

References (77)

1. Ala-Aho R, Johansson N, Grenman R, Fusenig NE, Lopez-Otin C, and Kahari VM (2000). Inhibition of collagenase-3 (MMP-13) expression in transformed human keratinocytes by interferon-gamma is associated with activation of extracellular signal-regulated kinase-1, 2 and STAT1. Oncogene 19:248-257.
2. Anim JT, Udo C, and John B (1998). Characterization of inflammatory cells in benign prostatic hyperplasia. Acta Histochem 100:439-449.
3. Bartsch G, Keen F, Daxenbichler G, Marth C, Margreiter R, Brungger A, Sutter T, and Rohr HP (1987). Correlation of biochemical (receptors, endogenous tissue hormones) and quantitative morphologic (stereologic) findings in normal and hyperplastic human prostates. J Urol 137:559-564.
4. Bauvois B, Roillard D, Sanceau J, and Wietzerbin J (1992). IFN-gamma and transforming growth factor-beta 1 differently regulate fibronectin and laminin receptors of human differentiating monocytic cells. J Immunol 148:3912-3919.
5. Bertoletti A, D'Elios MM, Boni C, De Carli M, Zignego AL, Durazzo M, Missale G, Penna A, Fiaccadori F, Del Prete F, and Ferrari C (1997). Different cytokine profiles of intrahepatic T cells in chronic hepatitis B and hepatitis C virus. Gastroenterology 112:193-199.
6. Berhoff E, Vogel J, Benz M, Giefer T, Wernert N, and Pfeifer U (1996). Stromal nodules in benign prostatic hyperplasia. Eur Urol 29:345-354.
7. Bierhoff E, Walljasper U, Hofmann D, Vogel J, Wernert N, and Pfeifer U (1997). Morphological analogies of fetal prostate stroma and stromal nodules in BPH. Prostate 31:234-240.
8. Ceponis PJ, Botelho F, Richards CD, and McKay DM (2000). Interleukins 4 and 13 increase intestinal epithelial permeability by a phosphatidylinositol 3-kinase pathway. Lack of evidence for STAT 6 involvement. J Biol Chem 275:29132-29137.
9. Chiaramonte MG, Donaldson DD, Cheever AW, and Wynn TA (1999). An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J Clin Invest 104:777-785.
10. Chung KY, Agarwal A, Uitto J, and Mauviel A (1996). An AP-1 binding sequence is essential for regulation of the human alpha2(I) collagen (COL1A2) promoter activity by transforming growth factor-beta. J Biol Chem 271:3272-3278.
11. Del Prete GF, De Carli M, Ricci M, and Romagnani S (1991). Helper activity for immunoglobulin synthesis of T helper type 1 (Th1) and Th2 human T cell clones: The help of Th1 clones is limited by their cytolytic capacity. J Exp Med 174:809-813.
12. Del Prete GF, Maggi E, and Romagnani S (1994). Human Th1 and Th2 cells: Functional properties, mechanisms of regulation, and role in disease. Lab Invest 70:299-306.
13. Dohm G (1991). Hyperplasie und sogenannte atypische Hyperplasie der Prostata. In: Dörr W, Seifert G, editors. Pathologie der männlichen Genitale. Berlin, Heidelberg, New York. London: Springer-Verlag, 480.
14. Doucet C, Brouty-Boye D, Pottin-Clemenceau, Canonica GW, Jasmin C, and Azzarone B (1998). Interleukin (IL) 4 and IL-13 act on human lung fibroblasts. J Clin Invest 101:2129-2139.
15. Dufort F, Rheault P, Huang XF, Soucy P, and Luu-The V (1999). Characteristics of a highly labil human type 5 17[beta]-hydroxysteroid dehydrogenase. Endocrinology 140:568-574.
16. Eickelberg O (2001). Endless healing: TGF-b, SMADs, and fibrosis. FEBS Lett 506:11-14.
17. El-Alfy M, Luu-The V, Huang XF, Berger L, Labrie F, and Pelletier G (1999). Location of type 5 17[beta]-hydroxysteroid dehydrogenase, 3[beta]-hydroxysteroid dehydrogenase and androgen receptor in the human prostate by in situ hybridisation and immunocytochemistry. Endocrinology 140:1481-1491.
18. Ferrick DA, Schrenzel MD, Mulvania T, Hsieh B, Ferlin WG, and Lepper H (1995). Differential production of interferon-gamma and interleukin-4 in response to Th1- and Th2-stimulating pathogens by gamma delta T cells in vivo. Nature 19:255-257.
19. Franks LM (1976). Benign prostatic hyperplasia: Gross and microscopic anatomy. In: Grayhack JT, Wilson JD, Scherbenske MJ, editors: Benign Prostatic Hyperplasia 1976. Department of Health, Education and Welfare (NIH) Publication. Washington: US Government Printing Office, 76-1113.
20. Gingras S and Simard J (1999). Induction of 3[beta]-hydroxysteroid dehydrogenase/isomerase type 1 expression by interleukin-4 in human normal prostate epithelial cells, immortalized keratocytes, colon, and cervix cancer cell lines. Endocinology 140:4573-4584.
21. Griffiths K (Chairman), Akaza H, Eaton CL, El Etreby M, Habib F, Lee C, Partin AW, Coffey DS, Sciarra F, Steiner GE, and Tenniswood MP (1993). Regulation of prostatic growth. In: Cockett ATK, Khoury S, Aso Y, Chatelain C, Denis L, Griffiths K, Murphy G, editors: 2nd International Consultation on Benign Prostatic Hyperplasia (BPH), 49-75.
22. Griffiths K (Chairman), Coffey DS, Cockett ATK, Sant Agnese A, Ichikawa T, Krieg M, Lee C, McKeehan W, Schalken J, Sciarra F, Steiner GE, Sigimura Y, and Yamanaka H (1996). Regulation of prostatic growth. In: Cockett ATK, Khoury S, Aso Y, Chatelain C, Denis L, Griffiths K, Murphy G, editors: 3rd International Consultation on Benign Prostatic Hyperplasia (BPH), 73-115.
23. Higashi K, Kouba DJ, Song YL, Uitto J, and Mauviel A (1998). A proximal element within the human alpha 2(I) collagen (COL1A2) promoter, distinct from the tumor necrosis factor-alpha response element, mediates transcriptional repression by interferon-gamma. Matrix Biol 16:447-456.
24. Ignotz RA, Endo T, and Massague J (1987). Regulation of fibronectin and type I collagen mRNA levels by transforming growth factor-beta. J Biol Chem 262:6443-6446.
25. Inagaki Y, Truter S, and Ramirez F (1994). Transforming growth factor-beta stimulates alpha 2(I) collagen gene expression through a cis-acting element that contains an Sp1-binding site. J Biol Chem 269:14828-14834.
26. Jimenez SA, Varga J, Olsen A, Li L, Diaz A, Herhal J, and Koch J (1994). Functional analysis of human alpha 1(I) procollagen gene promoter. Differential activity in collagen-producing and -nonproducing cells and response to transforming growth factor beta 1. J Biol Chem 269:12684-12691.
27. Jung T, Schauer U, Heusser C, Neumann C, and Rieger C (1993). Detection of intracellular cytokines by flow cytometry. J Immunol Methods 159:197-207.
28. Kahari VM, Chen YQ, Su MW, Ramirez F, and Uitto J (1990). Tumor necrosis factor-alpha and interferon-gamma suppress the activation of human type I collagen gene expression by transforming growth factor-beta 1. Evidence for two distinct mechanisms of inhibition at the transcriptional and posttranscriptional levels. J Clin Invest 86:1489-1495.
29. Kohnen PW and Drach GW (1979). Patterns of inflammation in prostatic hyperplasia: A histologic and bacterialogic study. J Urol 121:755-760.
30. Kramer G, Steiner GE, Sokol P, Handisurya A, Klingler HC, Maier U, Foldy M, and Marberger M (2001). Local intratumoral tumor necrosis factor-alpha and systemic IFN-alpha 2b in patients with locally advanced prostate cancer. J Interferon Cytokine Res 21:475-484.
31. Kramer G, Steiner GE, Handisurya A, Stix U, Haitel A, Knerer B, Gessl A, Lee Ch, and Marberger M (2002). Increased expression of lymphocyte-derived cytokines in benign hyperplastic prostate tissue, identification of the producing cell types and effect of differentially expressed cytokines on stromal cell proliferation. Prostate 52:43-58.
32. Labrie F, Dupont A, and Belanger A (1985). Complete androgene blockade for the treatment of prostate cancer. In: De Vita S, Hellman S, and Rosenberg SA editors. Important Advances in Oncology. Philadelphia: Lippincott, 193-217.
33. Labrie F, Simard J, Luu-The V, Pettelier G, Belghmi K, and Belanger A (1994). Structure, regulation and role of 3[beta]-hydroxysteroid dehydrogenase, 17[beta]-hydroxysteroid dehydrogenase and aromatic enzymes in the formation of sex steroids in classical and peripheral intracrine tisues. Bailleries Clin Endocrinol Metab 8:451-474.
34. Labrie F, Luu-The V, Lin SX, Labrie C, Simard J, Breton R, and Belanger A (1997). The key role of 17[beta]-hydroxysteroid dehydrogenase in sex steroid biology. Steroids 62:148-158.
35. Lee C, Sintich SM, Mathews EP, Shah AH, Kundu SD, Perry KT, Cho JS, Ilio KY, Cronauer MV, Janulis L, and Sensibar JA (1999). Transforming growth factor-[beta] in benign and malignant prostate. Prostate 39:285-290.
36. Lee C, Cockett A, Cussenot O, Griffiths K, Isaacs W, Schalken J, Buttyan R, Prins G, and Steiner GE (2001). Regulation of prostatic growth. In: Chatelian C, Denis L, Foo KT, Khoury S, and McConnell J, editors. 5th International Consultation on Benign Prostatic Hyperplasia (BPH):81-111.
37. Lin HK, Jez JM, Schlegel BP, Peehl DM, Pachter JA, and Penning TM (1997). Expression and characterization of recombinant type 2 3[alpha]-hydroxysteroid dehydrogenase (HSD) from human prostate: Demonstration of bifunctional 3[alpha]/17[alpha]-HSD activity and cellular distribution. Mol Endocrinol 11:1971-1984.
38. Meazza R, Basso S, Gaggero A, Detotero D, Trentin L, Pereno R, Azzarone B, and Ferrini S (1998). Interleukin (IL)-15 induces survival and proliferation of the growth factor-dependent acute myeloid leukemia M-07e through the IL-2 receptor β/γ. Int J Cancer 78:189-195.
39. Maini A, Hillman G, Haas GP, Wang CY, Montecillo E, Hamzavi F, Pontes JE, Leland P, Pastan I, Debinski W, and Ruri RJ (1997). Interleukin-13 receptors on human prostate carcinoma cell lines represent a novel target for a chimeric protein composed of IL-13 and a mutated form of pseudomonas exotoxin. J Urol 158:948-953.
40. Marie O, Thillaye-Goldenberg B, Naud MC, and de Kozak Y (1999). Inhibition of endotoxin-induced uveitis and potentiation of local TNF-α and interleukin-6 mRNA expression by interleukin-13. Invest Opthalmol Vis Sci 40:2275-2282.
41. Matsushita K, Takenouchi T, Kobayashi S, Hayashi H, Okuyama K, Ochiai T, Mikata A, and Isono K (1996). HLA-DR antigen expression in colorectal carcinomas: Influence of expression by IFN-gamma in situ and its association with tumour progression. Br J Cancer 73:644-648.
42. McClinton S, Eremin O, and Miller ID (1990). Inflammatory infiltrate in prostatic hyperplasia: Evidence of a host response to intraprostatic spermatozoa? Br J Urol 65:606-610.
43. McCormick LL, Zhang Y, Tootell E, and Gilliam AC (1999). Anti-TGF-beta treatment prevents skin and lung fibrosis in murine sclerodermatous graft-versus-host disease: A model for human scleroderma. J Immunol 163:5693-5699.
44. Moore RA. Inflammation of the prostate gland (1937). J Urol 38:173.
45. Mosmann TR and Coffman RL (1989). Heterogeneity of cytokine secretion patterns and functions of helper T cells. Adv Immunol 46:111-147.
46. Mosmann TR and Sad S (1996). The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17:138-141.
47. Ogata H, Ford D, Kouttab N, King TC, Vita N, Minty A, Stoeckler J, Morgan D, Girasole C, Morgan JW, and Maizel AL (1998). Regulation of interleukin-13 receptor constituents on mature human B lymphocytes. J Biol Chem 273:9864-9871.
48. Oriente A, Fedarko NS, Pacocha SE, Huang SK, Lichtenstein LM, and Essayan DM (2000). Interleukin-13 modulates collagen homeostasis in human skin and keloid fibroblasts. J Pharmacol Exp Ther 292:988-994.
49. Paschke R, Schuppert F, Taton M, and Velu T (1994). Intrathyroidal cytokine gene expression profiles in autoimmune thyroiditis. J Endocrinol 141:309-315.
50. Postlethwaite AE, Holness MA, Katai H, and Raghow R (1992). Human fibroblasts synthesize elevated levels of extracellular matrix proteins in response to interleukin 4. J Clin Invest 90:1479-1485.
51. Romagnani S (1997). The Th1/Th2 paradigm. Immunol Today 18:263-266.
52. Ruth JH, Warmington KS, Shang X, Lincoln P, Evanoff H, Kunkel SL, and Chensue SW (2000). Interleukin 4 and 13 participation in mycobacterial (type-1) and schistosomal (type-2) antigen -elicited pulmonary granuloma formation: Multiparameter analysis of cellular recruitment, chemokine expression and cytokine networks. Cytokine 12:432-444.
53. Sad S and Mosmann TR (1994). Single IL-2-secreting precursor CD4 T cell can develop into either Th1 or Th2 cytokine secretion phenotype. J Immunol 153:3514-3522.
54. Sad S, Marcotte R, and Mosmann TR (1995). Cytokine-induced differentiation of precursor mouse CD8+ T cells into cytotoxic CD8+ T cells secreting Th1 or Th2 cytokines. Immunity 2:271-279.
55. Schmidt-Graeff A, Desmouliere A, and Gabbiani G (1994). Heterogeneity of myofibroblasts phenotypic features: An example of fibroblastic cell plasticity. Virchows Arch 425:3-24.
56. Simard J, Durocher F, Mebarki F, Turgeon C, Sanchez R, Labrie Y, Couet J, Trudel C, Rheaume E, Morel Y, Luu-The V, and Labrie F (1996). Molecular biology and genetics of the 3 beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase gene family (Review). J Endocrinol 150(Suppl):189-207.
57. Sintich SM, Steinberg J, Kozlowski JM, Lee C, Pruden S, Sayeed S, and Sansibar JA (1999). Cytotoxic sensitivity to tumor necrosis factor-[alpha] in PC3 and LNCaP prostatic cancer cells is regulated by extracellular levels of SGP-2 (clusterin). Prostate 39:87-93.
58. Stearns ME, Rhim J, and Wang M (1999a). Interleukin 10 (IL-10) inhibition of primary human prostate cell-induced angiogenesis: IL-10 stimulation of tissue inhibitor of metalloproteinase-1 and inhibition of matrix metalloproteinase (MMP)-2/MMP-9 secretion. Clin Cancer Res 5:189-196.
59. Stearns ME, Garcia WU, Fudge K, Rhim J, and Wang Min (1999b). Role of interleukin 10 and transforming growth factor b1 in the angiogenesis and metastasis of human prostate primary tumor lines from orthopic implants in severe combined immunodeficiency mice. Clin Cancer Res 5:711-720.
60. Steiner G, Gessl A, Kramer G, Schöllhammer A, Förster O, and Marberger M (1994). Phenotype and function of peripheral and prostatic lymphocytes in patients with benign prostatic hyperplasia. J Urol 151:480-484.
61. Steiner G, Newman M, Paikl D, Stix U, Memaran-Dagdar N, Lee C, and Marberger M (2003). Expression and function of proinflammatory interleukin (IL)-17 and IL-17 receptor in normal, benign hyperplastic and malign prostate. Prostate. In press.
62. Steiner G, Tohidast-Akrad M, Witzmann G, Vesely M, Studnicka-Benke A, Gal A, Kunaver M, Zenz P, and Smolen JS (1999). Cytokine production by synovial T cells in rheumatoid arthritis. Rheumatology 38:202-213.
63. Theyer G, Kramer G, Assmann I, Sherwood E, Preinfalk W, Marberger M, Zechner O, and Steiner G (1992). Phenotypic characterization of infiltrating leukocytes in BPH. Lab Invest 66:96-107.
64. van den Berg JG, Aten J, Anwar Chand M, Claessen N, Dijking L, Wijdenes J, Lakkis FG, and Weening JJ (2000). Interleukin-4 and interleukin-13 act on glomerular visceral epithelial cells. J Am Soc Nephrol 11:413-422.
65. van der Graaff WL, Prins APA, Niers TMH, Dijkmans BAC, and van Lier RAW (1999). Quantitation of interferon gamma- and interleukin-4-producing cells in synovial fluid and peripheral blood of arthritis patients. Rheumatology 38:214-220.
66. Varga J, Olsen A, Herhal J, Constantine G, Rosenblom J, and Jimenez SA (1990). Interferon-gamma reverses the stimulation of collagen but not fibronectin gene expression by transforming growth factor-beta in normal human fibroblasts. Eur J Clin Invest 20:487-493.
67. Vita N, Lefort S, Laurent P, Caput D, and Ferrara P (1995). Characterization and comparison of the interleukin 13 receptor with the interleukin 4 receptor on several cell types. J Biol Chem 24:3512-3517.
68. Wang M, Fudge K, Rhim JS, and Stearns ME (1996). Cytokine regulation of the matrix metalloproteinases and their inhibitors in human papillomavirus-transformed human prostatic tumor cell lines. Oncol Res 8:303-315.
69. Willheim M, Ebner C, Baier K, Kern W, Schrattbauer K, Thien R, Kraft D, Breiteneder H, Reinisch W, and Scheiner O (1997). Cell surface characterization of T lymphocytes and allergen-specific T cell clones: Correlation of CD26 expression with T(H1) subsets. J Allergy Clin Immunol 100:348-355.
70. Willheim M, Thien R, Schrattbauer K, Bajna E, Holub M, Gruber R, Baier K, Pietschmann P, Reinisch W, Scheiner O, and Peterlik M (1999). Regulatory effects of 1alpha, 25-dihydroxyvitamin D3 on the cytokine production of human peripheral blood lymphocytes. J Clin Endocrinol Metab 84:3739-3744.
71. Woods JM, Katschke KJ Jr, Tokuhira M, Kurata H, Arai KI, Campbell PL, and Koch AE (2000). Reduction of inflammatory cytokines and prostaglandin E2 by IL-13 gene therapy in rheumatoid arthritis synovium. J Immunol 165:2755-2763.
72. Yamamura M, Uyemura K, Deans RJ, Weinberg K, Rea TH, Bloom BR, and Modlin RL (1991). Defining protective responses to pathogens: Cytokine profiles in leprosy lesions [published erratum appears in Science. 1992;255:5040]. Science 11:277-279.
73. Yano N, Endoh M, Naka R, Takemura F, Nomoto Y, and Sakai H (1996). Altered synthesis of interferon-γ receptor by peripheral blood mononuclear cells from patients with IgA nephropathy and non-IgA proliferative glomerulonephritis. J Clin Immunol 16:71-79.
74. Yuan W, Yufit T, Li L, Mori Y, Chen SJ, and Varga J (1999). Negative modulation of alpha1(I) procollagen gene expression in human skin fibroblasts: Transcriptional inhibition by interferon-gamma. J Cell Physiol 179:97-108.
75. Yufit T, Vining V, Wang L, Brown RR, and Varga J (1995). Inhibition of type I collagen mRNA expression independent of tryptophan depletion in interferon-gamma-treated human dermal fibroblasts. J Invest Dermatol 105:388-393.
76. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, Zhang Y, and Elias JA (1999). Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eptaxin production. J Clin Invest 103:779-788.
77. Zurawski G and de Vries JE (1994). Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells (Review). Immunol Today 15:19-26.