Interleukin-11 therapy selectively downregulates type I cytokine proinflammatory pathways in psoriasis lesions - PubMed (original) (raw)
Clinical Trial
. 1999 Dec;104(11):1527-37.
doi: 10.1172/JCI6910.
Affiliations
- PMID: 10587516
- PMCID: PMC409858
- DOI: 10.1172/JCI6910
Clinical Trial
Interleukin-11 therapy selectively downregulates type I cytokine proinflammatory pathways in psoriasis lesions
W L Trepicchio et al. J Clin Invest. 1999 Dec.
Erratum in
- J Clin Invest 2000 Feb;105(3):396
Abstract
Psoriasis is a chronic inflammatory skin disease in which epidermal hyperplasia results from skin infiltration by type I T lymphocytes and release of associated cytokines. A multifunctional cytokine, rhIL-11, modulates macrophage and type I T-lymphocyte function in cell culture and shows anti-inflammatory activity in animal models. We are testing subcutaneous delivery of rhIL-11 to patients with psoriasis in a phase 1 open-label dose-escalation clinical trial. Tissue was obtained from lesional and uninvolved skin before and during treatment with rhIL-11 and was examined by histology/immunohistochemistry and quantitative RT-PCR. Expression of over 35 genes was examined in all patients, and multiple genetic markers of psoriasis were identified. Expression of numerous proinflammatory genes was elevated in psoriatic tissue compared with nonlesional skin. Seven of 12 patients responded well to rhIL-11 treatment. Amelioration of disease by rhIL-11, as shown by reduced keratinocyte proliferation and cutaneous inflammation, was associated with decreased expression of products of disease-related genes, including K16, iNOS, IFN-gamma, IL-8, IL-12, TNF-alpha, IL-1beta, and CD8, and with increased expression of endogenous IL-11. We believe that this is the first study in humans to indicate that type I cytokines can be selectively suppressed by an exogenous immune-modifying therapy. The study highlights the utility of pharmacogenomic monitoring to track patient responsiveness and to elucidate anti-inflammatory mechanisms.
Figures
Figure 1
Photographs of psoriatic plaques undergoing resolution in 2 patients (A and B) before and after 8 weeks of treatment with rhIL-11.
Figure 2
Six-millimeter punch biopsies were obtained from lesional and nonlesional skin of a patient before treatment with rhIL-11 (pretreatment) and at weeks 1, 4, and 8 following daily treatment with 2.5 mg/kg of rhIL-11. Biopsies were equally divided for immunohistochemical analysis and RNA preparation. Frozen biopsies from pretreatment, week 4, and week 8 were sectioned and stained with antibodies to Ki67+, K16, CD3, CD8, and ICAM-1. Enlargements of ICAM-1 staining (boxes) show elimination of its production by epidermal keratinocytes during IL-11 administration (large arrows).
Figure 3
RNA was prepared from nonlesional and lesional skin of 6 untreated psoriasis patients. The mRNA was amplified for the indicated genes by quantitative RT-PCR. Levels of RNA were normalized to HARP. Average expression levels of nonlesional and lesional skin for all 6 patients are presented ± SEM. *Statistically significant differences (P < 0.05) between nonlesional and lesional skin; filled box, lesion; shaded box, nonlesion.
Figure 4
Six-millimeter punch biopsies were obtained from lesional and nonlesional skin of a responding patient before treatment with rhIL-11 (pretreatment) and at weeks 1, 4, and 8 following daily treatment with 2.5 mg/kg of rhIL-11. Biopsies were equally divided for immunohistochemical analysis and RNA preparation. RNA was prepared from nonlesional skin and lesional skin from pretreatment, week-1, week-4, and week-8 biopsies. The mRNA for IL-12 p40, IFN-γ, TNF-α, iNOS, CD8, IL-8, IL-4, and K16 were amplified by quantitative RT-PCR. Levels of mRNA were normalized to HARP to control for variations in starting RNA amounts.
Figure 5
RNA was prepared from nonlesional skin biopsies and lesional skin biopsies of 12 patients before treatment (pretreatment) and at week 1, week 4, and week 8 following daily treatment with 2.5 or 5.0 mg/kg of rhIL-11. Quantitative RT-PCR was performed on individual samples for the indicated genes. Gene expression levels were normalized to HARP. Levels of gene expression observed in the nonlesional skin of each patient were arbitrarily set to equal 1, and the fold change in expression in lesional skin before and after treatment with rhIL-11 over nonlesional skin was calculated. Average fold change for rhIL-11–responding (n = 7) and rhIL-11–nonresponding (n = 5) patients was calculated. Data are presented as the average fold change over nonlesional skin ± SEM. *Statistically significant differences between pretreatment and rhIL-11 treatment (P < 0.05); #statistically significant differences between responder and nonresponder pretreatment lesions (P < 0.05).
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References
- Greaves MW, Weinstein GD. Treatment of psoriasis. N Engl J Med. 1995;332:581–588. - PubMed
- Weinstein, G.D., and Kreuger, J.G. 1994. Overview of psoriasis. In Therapy of moderate to severe psoriasis. G.D. Weinstein and A.B. Gottlieb, editors. National Psoriasis Foundation. Portland, OR. 1–22.
- Gottlieb AB, et al. Studies of the effect of cyclosporine in psoriasis in vivo: combined effects on activated T lymphocytes and epidermal regenerative maturation. J Invest Dermatol. 1992;98:302–309. - PubMed
- Gottlieb SL, et al. Response of psoriasis to a lymphocyte-selective toxin (DAB389IL-2) suggests a primary immune but not keratinocyte pathogenic basis. Nat Med. 1995;1:442–447. - PubMed
- Bachelez H, et al. Treatment of recalcitrant plaque psoriasis with a humanized non-depleting antibody to CD4. J Autoimmun. 1998;11:53–62. - PubMed
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