CYTOKINE PROFILE IN AUTOSOMAL DOMINANT POLYCYSTIC KIDNEY DISEASE. M. Merta 1, V. Tesa? 1, T. Zima 2, M. 3irsa ~, R. Ry~,ava ~, J. Z.
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1 Vol. 41, No. 3, March 1997 Pages CYTOKINE PROFILE IN AUTOSOMAL DOMINANT POLYCYSTIC KIDNEY DISEASE M. Merta 1, V. Tesa? 1, T. Zima 2, M. 3irsa ~, R. Ry~,ava ~, J. Z.abka ~ ~lst Medical Department, ~lst Institute of Biochemistry, 1st Faculty of Medicine, Charles University, U nemocnice 2, CZ , Prague 2, Czech Republic Received Novembcr 28, 1996 Received after revision January 2, 1997 Summary To elucidate the pathogenetic mechanism of renal parenchymal injury in autosomal dominant polycystic kidney disease (ADPKD) patients, typically characterized by renal cystic changes paralleled by interstitial inflammation and gradual fibrotic changes, the role of selected inflammatory mediators was evaluated in a group of ADPKD patients with normal glomerular filtration rate. The plasma concentrations of IL-6, IL-8, ICAM-1 and VCAM-1 (which may reflect systemic response to inflammation/infection) were increased in the ADPKD patient group. Coupled with decreased urinary excretion of the IL-1 receptor antagonist (which exerts an anti-inflammatory role), these results suggest that even in overt infection free status, the proinflammatory system is more activated and anti-inflammatory defence system weakened in ADPKD subjects. Our data support the current view that cytokines are candidate contributors to pathogenesis of ADPKD. Key words: autosomal dominant polycystic kidney disease; cytokines; chronic renal failure; cysts Introduction Autosomal dominant polycystic kidney disease (ADPKD), the most frequent renal hereditary disease, is distinguished by multiorgan affection and gradual progression to chronic renal failure. Two ADPKD genes have been identified recently; their hypothetical products, polycystins, are intensively investigated. The renat cysts are derived from different nephron segments, 1but the underlying mechanism by which cysts form remains unclear. Unlike normal renal epithelial cells, human ADPKD cells grown in culture can form cysts, suggesting that the genetic defect directly promotes cyst formation (1). The hypothetical primary defect in ADPKD, abnormal cellular differentiation and maturation (1,2), could promote cyst /97/ Copyright by Academic Press Australia All rights of reproduction in any j?jrm reserved.
2 VOI. 41, No. 3, 1997 formation via several possible mechanisms including unregulated epithelial cell growth and abnormal targeting of cell proteins (3). Polycystin is probably involved in adhesive protein-protein interactions (4,5); due to some abnormal polycystin function an impairment of cell-cell and/or cell-matrix interactions could lead to abnormal epithelial cell differentiation and the various phenotypic expressions of ADPKD. Cysts in ADPKD arise in a minority of nephrons (6,7) and are thought to lead to renal failure by compressing adjacent normal parenchyma-a view being not currently supported by histological observations. Examination of renal tissue from ADPKD patients suggests that progressive renal failure in ADPKD correlates closely with the development of vascular sclerosis and interstitial fibrosis (8). Disclosure of mechanisms of early fibrotic and vascular changes (arterial hypertension, infection, cyst growth, or other factors) would substantially help to set up rational management and therapeutical approach. Besides morphological evidence, not easily available due to the character of the cystic disease, an indirect method might reflect fibrogenesis and vascular changes. In this setting, cytokines have been suggested as candidate contributors to the morbidity and pathogenesis of ADPKD (9). The present study addresses the role of some cytokines and other inflammatory mediators in the pathogenesis of fibrotic changes in ADPKD patients. Patients and methods Patients The study group consisted of randomly selected patients with ADPKD with preserved renal functions (glomerular filtration rate within normal range). In the ADPKD group 3 patients suffered from mild arterial hypertension. The control group consisted of healthy volunteers. Subjects from both groups were free of infection, on normal, nonrestricted diet. Clinical data are summarized in Table 1. Cytokine collection and determination Blood and urine were obtained from fasting subjects under basal conditions in the morning. In blood and urine samples from all patients concentrations of following mediators were determined: (1) interleukins 6 and 8 (IL-6, IL-8,), (2) interleukin-1 receptor antagonist (IL-1Ra), (3) intracellular adhesion molecule 1 and vascular adhesion molecule I(ICAM-1, VCAM-1). Urine production (elimination) of mediators was calculated and compared as excretion fraction. Statistical methods The results are expressed as means + standard deviation. Differences in cytokine concentration and production between ADPKD and control groups were 620
3 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL Table 1. Clinical.data of study groups ADPKD group Control group n= 10 n--9 Age (years) _+ 3,55 Sex 7f, 3m 6f, 3m Creatininemia (tjmol/l) Arterial hypertension 3 0 tested using ANOVA statistical programme. A value of p < 0.05 was considered significant. Results Table 2 shows that the plasma concentrations of IL-6 and IL-8 were significantly increased in the ADPKD group, but their urinary excretion did not differ from the control group. Plasma concentrations of adhesion molecules were significantly higher in the ADPKD group than in the control group; differences in their urinary excretion were markedly weaker (ICAM-1) or insignificant (VCAM-1). Strikingly higher urinary excretion of IL-1Ra was found in ADPKD, whereas no significant differences were observed in their plasma levels. Patients with arterial hypertension did not form any subgroup differing significantly from other ADPKD patients without hypertension as to plasma concentrations or urinary excretion of selected mediators. Discussion Release of cytokines is involved, as an integral part, in the current hypothesis of the development of terminal renal failure (10, 11). Chronic inflammation generally precedes the development of fibrosis and inflammatory cytokines are important mediators of fibrogenesis (12). While a link between tubular injury, tubule-derived cytokines, interstitial cell infiltrate and tubulointerstitial pathology in the progression of human renal disease is becoming quite convincing (13), evidence and/or estimation of the extent of such a process in ADPKD is missing. Likewise, little is known about the possible impact of cystic changes affecting tubular cells (especially the proximal ones), which are presumed to produce a number of proinflammatory 621
4 Table 2. Plasma concentrations and urinary excretion of selected mediators in ADPKD and control groups Plasma cytokine concentration/ ADPKD Controls Statistical Urinary excretion fraction n = 10 n = 9 significance Plasma IL p < (pg/ml) Excretion fraction IL n.s. Plasma IL p < (pg/ml) Excretion fraction IL n.s. Plasma ICAM p<o.01 (ng/ml) Excretion fraction ICAM p < 0.05 Plasma VCAM ] p < 0.01 (ng/ml) Excretion fraction VCAM _ n.s. Plasma IL-lra _ n.s. (pg/ml) Urinary excretion IL-lra 10.6 z p < 0.01 (pg/mol creatinine) molecules involved in interstitial inflammation and scarring (14). Two points should be stressed in connection with ADPKD: primary parenchymal injury is of tubulointerstitial origin and gradual pathogenetic steps and tissue loss (partly due to its hereditary nature) progress and develop extremely slowly in comparison with many immunologically mediated renal diseases. In this context changes in the production (and degradation) of some mediators might be expected to be less pronounced in ADPKD than in other more rapidly progressing diseases. We have demonstrated that some selected mediators of cytokine nature which are thought to play some role in the inflammatory status of the organism are up-regulated in patients with ADPKD. Especially IL-6 has a vast spectrum of biological activities, acts on various cell types and has been proposed to be associated with 622
5 pathogenesis of certain disease conditions, including inflammatory reactions-(15), whereas IL-8 enhances neutrophil activation, chemotactic stimulation for endothelial cells acting in angiogenesis and proliferation of smooth muscle cells. IL-1 is a proinflammatory cytokine which exerts a wide range of biological effects. While its importance in acute inflammatory response is well established, its role in fibrosis is tess clear (16). IL-1Ra causes blokade of IL-1 effect. Increased tubular (and/or vascular) expression of ICAM-1 and VCAM-1 has been observed in a large range of nephropathies, possibly reflecting non-specific tubular damage; and are presumably induced by different cytokines (IL-1, tumour necrosis factor). When evaluating our results, factors possibly influencing cytokine activity have to be considered. The activity of a cytokine is regulated in part through regulation of their receptors; the cytokine receptors may be modulated by other cytokines and also by several pathological and physiological stimuli; some cytokines are capable of modulating their own receptors. Another factor could be renal failure, which could also interfere with the cytokine function; however, data available on spontaneous secretion of monokines in patients with impaired renal function are contradictory and difficult to interpret (17). Using polycional antibodies raised against polycystin, this gene product was found to lacalize to the extracellular matrix of kidney, liver and cerebral blood vessels. Polycystin was highly expressed in the mesenchyme of developing kidney and liver and transiently in the glomerulus; in adult normal kidney polycystin was restricted to perivascular and periglomerular matrix, in addition in adult polycystic kidney antibody staining was also observed in the interstitium between cysts (18). It seems likely that polycystin acts as an extracellular protein, inluencing renal (and hepatic) morphogenesis. Taken together with previous observations of alterations in growth regulation along with increased expression of proto-oncogenes (19) changes in extracellular matrix, endogenous growth factors and other mediators are presumed to play a key role in renal cystogenesis and progression of impairment of renal function in ADPKD (20). Our results support these suggestions. Acknowledgement : This work was supported by grant no of Czech Ministry of Health. 623
6 BIOCHEMISTRYQnd MOLECULAR BIOLOGY INTERNATIONAL References 1. Woo, D.D., Miao, S.Y., Pelayo, JC., Woolf, A.S., (1994) Nature, 368, Grantham, J.J., (1993) J. Am. Soc. Nephrol., 3, Grantham, J.J., Ye, M., Gattone, V.H., Sullivan, L.P.(1995) J. Clin. Invest., 95, Hughes, J., Ward, C.J., Peral, B., Aspinwall, R., Clark, K., San Maillan, J.L.., Gamble, V., Harris, P.C.(1995) Nat. Genet, 10, The International Polycystic Kidney Disease Consortium, (1995) Cell, 81, Gardner, K.D. Jr., Glew, R.H., Evan, A.P.,Mc Ateer, J.A., Bernestein (1994) J. Am. J. Physiol., 266, F Gardner, K.D.Jr., Burnside, J.S., Skipper, B.J., (1992) Kidney Int., 42, Zeier, M., Fehrenbach, P., Geberth, S., (1992) Kidney Int., 42, Gardner, K. D. Jr., Burnside, J. S., Elzinga, LW., Locksley, R.M. (1991) Kidney Int., 39, Noronha, I.L, Niemir, Z., Stein, H., Waldherr, R., (1995) Nephrol. Dial. Transplant. 10, Stahl, R.A.K. (1995) Nephrol. Dial. Transplant., 10, Strutz, F. (1995) Nephrol. Dial. Transptant.,lO, Ong, A.C.M., Fine, UG. (1994) Nephrol. Dial. Transplant., 9, Burton, C.J., Walls, J. (1996) Nephrol. Dial. Transplant., 11, Ohta, K., Takano, N., Seno, A., Yachie, A., Miyawaki, T. (1992) Clinical Nephrology, 38, Nikolic-Paterson, D.J., Main, I.W., Tesch, G.H.,Lan, H.Y., Atkins, R.C.(1996) Kidney Int., 49, Suppl. 54, Leimenstoll, G., Zabel, P., Birkner, T., Heyl, K., Preusse, D. (1994) Nephrol. Dial. Transplant., 9, Bacallao, R.(1995) Nature Medicine, 1, Wilson, P.D., Du, J., Norman, J.T.(1993) Euro. J. Cell. Biol., 61, Adelsberg, J.S., Frank, D. (1995) Nature Medicine, 1,
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