Alcohol Dehydrogenase (ADH) Isoenzymes and Aldehyde Dehydrogenase (ALDH) Activity in the Sera of Patients with Gastric Cancer
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1 Dig Dis Sci (2008) 53: DOI /s ORIGINAL PAPER Alcohol Dehydrogenase (ADH) Isoenzymes and Aldehyde Dehydrogenase (ALDH) Activity in the Sera of Patients with Gastric Cancer Wojciech Jelski Æ Lech Chrostek Æ Bogdan Zalewski Æ Maciej Szmitkowski Received: 6 June 2006 / Accepted: 24 November 2007 / Published online: 30 January 2008 Ó Springer Science+Business Media, LLC 2007 Abstract Background Investigations have shown that alcohol dehydrogenase (ADH) and aldehyde dehydrogenase (ALDH) are present in some cancer cells and can play role in carcinogenesis. In recent experiments we found elevated alcohol dehydrogenase class IV activity in gastric cancer cells. This suggests these changes may be reflected by enzyme activity in the serum. Aim In this work we measured the activity of alcohol dehydrogenase isoenzymes and aldehyde dehydrogenase in the sera of patients with gastric cancer matched on gender. Methods Serum samples were taken for routine biochemical investigation from 55 patients with gastric cancer, before treatment, and from 55 control subjects. Total ADH activity was measured photometrically and ALDH activity by a fluorimetric method. For measurement of the activity of class I isoenzymes we used a fluorimetric method, with class-specific fluorogenic substrates. The activity of class III and IV alcohol dehydrogenase was measured photometrically. Results The activity of the class IV ADH isoenzyme was significantly higher in the sera of patients with gastric cancer. The median activity of this isoenzyme in the total cancer group was approximately 47% higher (7.45 mu/l) than the control level (5.08 mu/l). For this reason total ADH activity was also significantly increased. The activities of other tested ADH isoenzymes and ALDH were unchanged. Conclusion Changes in the activity of, especially, class IV ADH in the sera of patients with gastric cancer seems to be caused by release of the isoenzyme from cancer cells. W. Jelski (&) L. Chrostek B. Zalewski M. Szmitkowski Department of Biochemical Diagnostics, Medical University of Bialystok, Waszyngtona 15, Bialystok , Poland wjelski@amb.edu.pl Keywords Alcohol dehydrogenase isoenzymes Aldehyde dehydrogenase Gastric cancer Introduction The human gastric mucosa expresses isoenzymes of three classes of alcohol dehydrogenase (ADH) I, III, and IV [1, 2]. Gastric ADH is responsible for most ethanol metabolism in human gastric cells and plays an important role in the first-pass metabolism of ethanol. Gastrointestinal ADH isoenzymes are a metabolic barrier against ethanol produced from carbohydrates by bacterial fermentation and also against orally administered alcohol [3, 4]. The enzyme responsible for metabolism of acetaldehyde derived from ethanol oxidation in humans is aldehyde dehydrogenase (ALDH). Quantitative histochemical techniques have revealed that alcohol dehydrogenase activity is maximum in the most superficial part of the gastric mucosa and less in the deeper part of the stomach wall [5]. The mucosa is the location of the highest activity of ADH in the stomach, and the muscle layer of the mucosa and submucosa may also contain some enzyme activity. The activity of ADH isoenzymes depends on various factors including the morphology of the gastric mucosa [6]. In previous work we showed that ADH and its class I, III, and IV isoenzymes are present in gastric cancer cells [1]. The total activities of ADH and class IV isozymes were significantly higher in cancer tissues than in healthy mucosa [7]. ADH IV may play two important physiological roles, as a major contributor to first-pass metabolism of ethanol in stomach and involvement in the synthesis of retinoic acid. In this study we investigated the activity of alcohol dehydrogenase and its isoenzymes and the total activity of aldehyde dehydrogenase in the sera of patients with gastric cancer.
2 2102 Dig Dis Sci (2008) 53: Methods Patients The protocol was approved by the Human Care Committee of the Medical University in Bialystok, Poland (Approval No. R-I-003/2/2005). All patients gave informed consent to the examination. Serum samples were taken for routine biochemical investigations from 55 patients (34 males and 21 females, mean age of men 63, range 58 72; mean age of women 62, range years) with gastric cancer. All tumors were histologically verified as adenocarcinomas G2 pt 3. The tumors were classified in accordance with the staging of the 5th International Union Against Cancer (UICC). Pretreatment staging procedures included physical and blood examinations, colonoscopy, chest X-ray, and computerized tomography (CT). None of the patients had received chemotherapy or radiotherapy before serum collection. All of the patients drank alcohol moderately (weekly average consumption of 90 g ethanol or less). Serum samples were also obtained from 55 healthy adults aged years (men: 34, women: 21). None consumed any drug or alcohol. Biochemical assays Determination of total ADH activity Total ADH activity was measured photometrically with p-nitrosodimethylaniline (NDMA) as substrate [8]. The reaction mixture contained 0.1 ml serum, 1.8 ml of a 26 lmol/l solution of the substrate (100 ll) in 0.1 mol/l sodium phosphate buffer, ph 8.5, and 0.1 ml of a mixture containing 1.2 mol/l n-octanol (6.8 ll) and 5 mmol/l NAD (93.2 ll). Reduction of NDMA was monitored at 440 nm with a Shimadzu UV/VIS 1202 spectrophotometer (Shimadzu Europa, Duisburg, Germany). Determination of total ALDH activity ALDH activity was measured using the fluorimetric method based on oxidation of 6-methoxy-2-naphthaldehyde to the fluorescent 6-methoxy-2 naphthoate [9]. The reaction mixture contained 60 ll serum, 60 ll substrate, 20 ll 11.4 mmol/l NAD, and 2.8 ml 50 mmol/l sodium phosphate buffer, ph 8.5. The blank mixture also contained 50 ll of a 12 mmol/l solution of 4-methylpyrazole as a specific inhibitor of ADH activity. The fluorescence was read at an excitation wavelength of 310 nm and an emission wavelength of 360 nm on a Shimadzu RF-5301 spectrofluorimeter (Shimadzu Europa). Determination of class I ADH isoenzymes Class I alcohol dehydrogenase isoenzymes activity was measured using a fluorogenic substrate (4-methoxy-1- naphthaldehyde) in reduction reaction according to Wierzchowski et al. [10]. The assays were performed in a reaction mixture containing serum (60 ll), substrate (150 ll of 300 lmol/l), NADH (100 ll of 1 mmol/l) and 0.1 mol/l sodium phosphate buffer, ph 7.6 (2.69 ml) under conditions described elsewhere [11]. Measurements were performed with a Shimadzu RF-5301 spectrofluorimeter at an excitation wavelength of 316 nm and an emission wavelength of 370 nm. For evaluation of alcohol dehydrogenase activity two assays were carried out, one with substrate alone and one with 50 ll of a 12 mmol/l solution of 4-methylpyrazole as a specific inhibitor of the enzyme. Determination of class III ADH isoenzyme The assay mixture for class III alcohol dehydrogenase contained a serum (100 ll), formaldehyde as substrate (100 ll of 1 mmol/l), glutathione (100 ll of 1 mmol/l), NAD (240 ll of 1.2 mmol/l) in 0.1 mol/l NaOH glycine buffer, ph 9.6 [12]. The final volume was 2 ml. Reduction of NAD was monitored at 340 nm and 25 C with a Shimadzu UV/VIS 1202 spectrophotometer. Determination of class IV ADH isoenzyme The assay mixture (3 ml) for class IV alcohol dehydrogenase contained serum (50 ll), m-nitrobenzaldehyde as substrate (132 ll of 80 lmol/l), NADH (172 ll of 86 lmol/l), and 50 ll of a 12 mmol/l solution of 4-methylpyrazole in 0.1 mol/l sodium phosphate buffer, ph 7.5 [13]. Oxidation of NADH was monitored at 340 nm and 25 C with a Shimadzu UV/VIS 1202 spectrophotometer. Statistical analysis Preliminary statistical analysis (chi-squared test) revealed that the ADH and ALDH activities did not follow a normal distribution. Consequently, the Wilcoxon s test was used for statistical analysis. Data are presented as median, range, and mean. Statistically significant differences were defined as comparisons resulting in P \ 0.05.
3 Dig Dis Sci (2008) 53: Results The activities of alcohol dehydrogenase, aldehyde dehydrogenase, and isoenzymes of alcohol dehydrogenase in the sera are listed in Table 1. Total activity of alcohol dehydrogenase was significantly higher (40%) in patients with gastric cancer than in healthy subjects (P \ 0.001). The median total activity of ADH was 954 mu/l in the patients group and 682 mu/l in the control group. Analysis of ALDH activity did not indicate significant difference between the total tested group and healthy controls (P = 0.248). Comparison of ADH isoenzymes activities showed that the large difference was because of class IV ADH. The median activity of this class of isoenzyme in the cancer group was approximately 47% higher (7.45 mu/l) than the control level (5.08 mu/l). This increase was statistically significant (P \ 0.001). The other classes of ADH isoenzymes tested had higher activities in the serum of patients with cancer but the differences were not statistically significant in all patients groups (P [ 0.05). Significantly higher class IV ADH activity was found in the sera of men with cancer in comparison with men without cancer (P \ 0.001) and women with cancer when compared with women without cancer (P \ 0.001). In contrast, there were no marked differences in activities of other tested ADH isoenzymes between patients and control groups (men and women). Discussion Alcohol dehydrogenase was first described in the human stomach three decades ago [14]. Three different isoenzymes of ADH have been isolated from healthy gastric mucosa [15]. The morphology of the gastric mucosa is one factor that may influence stomach ADH activity. In our last study we showed that ADH and ALDH activities are present in healthy gastric mucosa and also in gastric cancer cells. In this investigation we observed that serum total alcohol dehydrogenase activity changed in the course of gastric cancer. The increase in the total activity of ADH was positively correlated with ADH IV, so the cause of the increase of serum total alcohol dehydrogenase in the course of gastric cancer is elevation of class IV ADH isoenzyme. Changes of other ADH isoenzyme activities were not significant. The marked increase of ADH IV isoenzyme in the sera of cancer patients may be explained by the high activity of this isoenzyme in cancer cells [7]. High activity of ADH IV is also characterized in healthy gastric mucosa [1]. Moreover ADH IV is localized in the superficial part of Table 1 ADH and ALDH activity in the sera of patients with gastric cancer Tested group ADH I (mu/l) ADH III (mu/l) ADH IV (mu/l) ADH total (mu/l) ALDH total (mu/l) Total (n = 55) Gastric cancer (age 54 72) Control (n = 55) (age 53 70) P = a P = a P \ a P \ a P = a Men (n = 34) Gastric cancer (age 58 72) Control (n = 34) (age 56 70) P = a P = a P \ a P \ a P = a Women (n = 21) Gastric cancer (age 54 70) Control (n = 21) (age 53 67) P = a P = a P \ a P \ a P = a P = b P = b P = b P = b P = b a Gastric cancer versus control; emboldening indicates the difference is significant b Men with gastric cancer versus women
4 2104 Dig Dis Sci (2008) 53: gastric mucosa. This class of ADH isoenzyme plays the most important role in the first-pass metabolism of ethanol in the stomach [2]. As described by other authors, class I ADH has very low activity but ADH II is absent in the gastric mucosa [2]. Class III ADH occurs in the stomach, but the kinetic properties of this isoenzyme indicate that it cannot be saturated by ethanol under physiological conditions [16]. The second possible explanation may be selective induction and release of class IV alcohol dehydrogenase from gastric cancer cells. The results of our previous study showed that only the activity of class IV ADH (the principal class of ADH isoenzymes in the stomach) was significantly higher in gastric cancer than in healthy mucosa. ADH IV also catalyzes the oxidation of retinol to retinal, the first step in the biosynthesis of retinoic acid. It is a principal mediator of the actions of retinoids required for maintaining epithelia in a differentiated state. The requirement of different extrahepatic tissues for retinoic acid is thought to be met largely by retinoic acid generated in situ from retinol. Disruption of elements of the retinoid homeostatic system has been identified in diverse cancers [17]. Differences between the activities of other tested classes of alcohol dehydrogenase isoenzymes in cancer cells and healthy mucosa were not statistically significant. In our opinion ADH III and ADH I are not secreted into the sera because these isoenzymes have low activity in cancer cells. For example in colorectal cancer the total activity of alcohol dehydrogenase and the class I of ADH were significantly higher than in healthy colon mucosa [9]. Therefore, the activity of class I alcohol dehydrogenase isoenzymes was significantly elevated in the serum of patients with colorectal cancer (unpublished data). In our previous study we found that the activity of ALDH was not different between gastric cancer cells and unchanged mucosa [7]. Serum levels of aldehyde dehydrogenase were, also, not significantly higher in patients with gastric cancer in comparison with the healthy group. In addition ALDH activity in the serum cancer patients was low compared with ADH activity. This would suggest low capability to remove acetaldehyde from the serum of these patients. The activities of alcohol dehydrogenase isoenzymes located in the gastric mucosa are conditioned by such factors as sex, age, medication taken, and the amount of alcohol intake. It is known that the activity of class IV alcohol dehydrogenase (stomach ADH) is significantly higher in men than in women [18, 19]. In our previous investigations we found a difference between the activity of this class of isoenzyme in the gastric cancer cells of males and females. In the sera of patients with gastric cancer, activity is higher in men than in women but the difference is not statistically significant. In future research these data may be used for evaluation of the usefulness of alcohol dehydrogenase in the diagnosis of gastric cancer. In conclusion, we can state that the increased activity of class IV alcohol dehydrogenase isoenzyme in the sera of gastric cancer patients seems to be caused by release of this isoenzyme from cancer cells. References 1. Jelski W, Chrostek L, Szmitkowski M, Laszewicz W (2002) The activity of class I, II, III and IV of alcohol dehydrogenase isoenzymes in gastric mucosa. Dig Dis Sci 47: Yin SJ, Liao CS, Wu CW, Li TT, Chen LL, Lai CI, Tsao TY (1997) Human stomach alcohol dehydrogenase and aldehyde dehydrogenase: comparison of expression pattern and activities in alimentary tract. Gastroenterology 112: Haber PS, Gentry T, Mak KM, Mirmiran-Yazdy SA, Greenstein RJ, Lieber CS (1996) Metabolism of alcohol by human gastric cells: relation to first-pass metabolism. Gastroenterology 111: Lim RT, Gentry RT Jr, Ito D, Yokoyama H, Baraona E, Lieber CS (1993) First-pass metabolism of ethanol is predominantly gastric. Alcohol Clin Exp Res 17: Maly IP, Arnold M, Krieger K, Zalewska M, Sasse D (1992) The intramucosal distribution of gastric alcohol dehydrogenase and aldehyde dehydrogenase activity in rats. Histochemistry 98: Moreno A, Pares A, Ortiz J, Enriquez J, Pares X (1994) Alcohol dehydrogenase from human stomach: variability in normal mucosa and effect of age, gender, ADH 3 phenotype and gastric region. Alcohol Alcohol 29: Jelski W, Chrostek L, Szmitkowski M (2007) The activity of class I, III and IV of alcohol dehydrogenase (ADH) isoenzymes and aldehyde dehydrogenase (ALDH) in the gastric cancer. Dig Dis Sci 52: Chrostek L, Jelski W, Szmitkowski M, Puchalski Z (2003) Alcohol dehydrogenase (ADH) isoenzymes and aldehyde dehydrogenase (ALDH) activity in the human pancreas. Dig Dis Sci 48: Jelski W, Zalewski B, Chrostek L, Szmitkowski M (2004) The activity of class I, II, III and IV of alcohol dehydrogenase (ADH) isoenzymes and aldehyde dehydrogenase (ALDH) in the colorectal cancer. Dig Dis Sci 49: Wierzchowski J, Dafeldecker WP, Holmquist B, Vallee BL (1989) Fluorimetric assay for isozymes of human alcohol dehydrogenase. Anal Biochem 178: Chrostek L, Jelski W, Szmitkowski M, Puchalski Z (2003) Gender-related differences in hepatic activity of alcohol dehydrogenase isoenzymes and aldehyde dehydrogenase in humans. J Clin Lab Anal 17: Koivusalo M, Baumann M, Uotila L (1989) Evidence for the identity of glutathione- dependent formaldehyde dehydrogenase and class III alcohol dehydrogenase. FEBS Lett 257: Dohmen K, Baraona E, Ishibashi H, Pozzato G, Moretti M, Matsunaga C, Fujimoto K, Lieber CS (1996) Ethnic differences in gastric r-alcohol dehydrogenase activity and ethanol first-pass metabolism. Alcohol Clin Exp Res 20: Hempel JD, Pietruszko R (1979) Human stomach alcohol dehydrogenase: isoenzyme composition and catalytic properties. Alcohol Clin Exp Res 3: Yin S-J, Wang M-F, Liao C-S (1990) Identification of human stomach alcohol dehydrogenase with distinctive kinetic properties. Biochem Int 22:
5 Dig Dis Sci (2008) 53: Kaiser R, Holmquist B, Vallee BL, Jornvall H (1991) Human class III alcohol dehydrogenase/glutathione-dependent formaldehyde dehydrogenase. J Protein Chem 10: Yin SJ, Chou CF, Lai CL, Lee SL, Han CL (2003) Human class IV alcohol dehydrogenase: kinetic mechanism, functional roles and medical relevance. Chem Biol Interact 1: Frezza M, Padova C, Pozzato G, Terpin M, Baraona E, Lieber CS (1990) High blood alcohol levels in women: the role of decreased gastric alcohol dehydrogenase activity and first-pass metabolism. Engl J Med 322: Harada S, Okubo T (1993) Investigated of alcohol dehydrogenase isozymes of biopsy gastric mucosa in Japanese. Alcohol Alcohol 28:59 62
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