Mutagenesis, Vol. 16, No. 3, 257-263,
May 2001
© 2001 UK Environmental Mutagen Society/Oxford University Press
Inducible protective processes in animal systems: VIII. Enhancement of adaptive response by nicotinamide
1 Department of Zoology, Manasagangotri, University of Mysore, Mysore, 570 006 and 2 Department of Applied Zoology, Jnanasahyadri, Kuvempu University, B.R. Project-577 115
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Abstract |
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The molecular mechanism of the adaptive response or inducible DNA repair process has not been clearly demonstrated in eukaryotic systems. The involvement of poly(ADP-ribose) polymerase (PARP), a DNA repair enzyme has been reported in the adaptive response (Shadley and Wolff, 1987
; Wiencke, 1987). Hence, the present studies were undertaken to understand the role of PARP in ethyl methanesulfonate (EMS)-induced adaptive response in mouse bone marrow cells by employing the inhibitor of this enzyme, nicotinamide. Inter-, pre- and post-treatments of nicotinamide with EMS were made. The results have revealed that there is a reduction in the frequencies of chromosomal aberrations compared with combined or challenge treatment at the different recovery times tested. These results are discussed with reference to the enhancement of the adaptive response by nicotinamide in mouse bone marrow cells. |
Introduction |
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The adaptive DNA repair process or inducible DNA repair pathway is a novel type of repair pathway among the several repair mechanisms known to date, wherein the cells pre-exposed to a low dose of a clastogen are more resistant to the damaging effects of a challenge dose of the same agent. This phenomenon, termed `the adaptive response', was first demonstrated by Samson and Cairns (1977) in Escherichia coli. Extensive reports are available on the existence of the adaptive response in prokaryotes and in in vitro eukaryotes using physical agents like X-rays,
-rays (Olivieri et al., 1984; Shadely and Wolff, 1987; Sankaranarayanan et al., 1989; Liazen Zhang, 1995; Ikushima et al., 1996; Wolff, 1996; Lankinen and Vilpo, 1997; Nikolai et al., 1998) and chemicals such as, N-methyl-N'-nitro-N-nitrosoguanidine (MNNG), methylnitrosourea (MNU), ethylnitrosourea (ENU) and mitomycin C (Samson and Schwartz, 1980; Kaina, 1982; Olivieri and Bosi, 1990; Mudrigal-Bujaidar et al., 1994; Kleczkowska and Althaus, 1996; Nikolova and Huttner, 1996).The same phenomenon was reported in the cells of higher plants by using alkylating and non-alkylating agents (Rieger et al., 1982, 1990; Baranczewski et al., 1997). We demonstrated the existence of adaptive response in grasshopper and mouse in vivo (Riaz Mahmood and Vasudev, 1990– 1993; Riaz Mahmood et al., 1996; Vasudev et al., 1997) and also in vitro in human lymphocytes (Harish et al., 1998). Although there are considerable data on the adaptive response, the molecular mechanism remains unclear. Different repair enzymes are implicated in this repair pathway. Poly(ADP-ribose) polymerase (PARP) is one such repair enzyme that has been reported to participate in DNA repair processes. PARP is a nuclear enzyme activated by DNA strand breaks induced by alkylating agents or X-rays (Cleaver et al., 1983; Chatterjee and Berger, 1994; Kleczkowska and Althaus, 1996). PARP upon activation catalyses of poly(ADP-ribosyl)ation of the various nuclear proteins and also that of PARP by utilizing NAD+ as substrate. Furthermore, the adaptive response was prevented in vitro, when inhibitors of PARP were administered 2 h after the adaptive treatment (Wiencke et al., 1986; Shadely and Wolff, 1987; Wiencke, 1987). These reports suggest the involvement of PARP in the adaptive response. Hence, in the present investigations, an attempt has been made using in vivo mouse bone marrow cells to understand the role of the PARP in ethyl methanesulfonate (EMS)-induced adaptive response. Nicotinamide, as an inhibitor of PARP (Purnell and Whish, 1980), has enhanced the EMS-induced adaptive response. The involvement of PARP in the adaptive response and the above results are discussed in this paper. |
Materials and methods |
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Animals
Male Swiss albino mice, 6–8 weeks old and weighing 25–30 g were used in the present studies.
Chemicals
The monofunctional alkylating agent, EMS (CAS-62-50-0) and the nicotinamide (N, CAS-98-92-0) were obtained from Sigma Chemical Company (USA). The EMS and nicotinamide were dissolved in 0.7% NaCl and distilled water, respectively, to obtain required concentrations. 0.5 ml of the fixed concentration was injected intraperitoneally. Freshly prepared chemical solutions were used. Two doses of EMS, 80 (conditioning, L) and 240 mg/kg body weight (challenge, H) were selected from the earlier experiments (Riaz Mahmood and Vasudev, 1993). Nicotinamide concentrations ranging from 5 to 50 mM/kg body weight were employed in the initial experiments to evaluate the toxicity (Table I). The results indicated that the lowest dose of 5 mM produces least toxicity when administered with combined treatments and at the same time the mitotic index was equivalent to controls when compared with higher doses. Hence, the dose of 5 mM/kg body weight was selected.
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Treatment schedule
EMS combined treatment
This was again selected from the previous experiments of Riaz Mahmood and Vasudev (1993), who have shown that the 8 h time lag (TL) between the conditioning and challenging treatment offered maximum protection with respect to the chromosomal aberrations in mouse bone marrow cells; thus exhibiting a peak of repair activity compared with other TLs. Therefore, the 8 h TL was selected for the present studies.
Nicotinamide inter-treatment
Nicotinamide inter-treatment was made during the period between the conditioning and challenging doses. As the 8 h TL was found to be at peak action or repair (Riaz Mahmood and Vasudev, 1993), this TL was used. Nicotinamide was injected 2 or 4 h after the conditioning dose. Then after 6 or 4 h they were challenged with the challenge dose of EMS.
Nicotinamide pretreatment
In this treatment schedule, animals received nicotinamide, 4 or 6 h prior to the conditioning dose of EMS and 8 h later they were challenged with the EMS high dose.
Nicotinamide post-treatment
Nicotinamide was given 6, 12 or 18 h after the combined treatment of EMS.
Slide preparation and chromosome analysis
Animals were killed by cervical dislocation at 24, 48 or 72 h recovery times (RTs) after the challenge dose. 0.5 ml of the 0.05% colchicine was injected into the animals 90 min prior to sacrifice. After the animals had been killed, the bone marrow was processed and slides were prepared by the routine air-dry technique (Evans et al., 1964). In brief, the femur bones were dissected out and cleaned. Then the bone marrow was flushed into 0.56% potassium chloride (hypotonic) solution with the help of 26 gauge needle attached to a 2 ml syringe. The suspension was incubated at 37°C for 30 min. After incubation, the cell suspension was centrifuged at 800 r.p.m. for 7 min. The supernatant was discarded. Then the fixative, methanol/acetic acid (3:1 v/v), was added to the pellet and mixed well. This suspension was centrifuged after 10 min. After fixing the cells three times, the pellet was resuspended in a 0.5 ml fixative. This suspension was dropped onto clean, non-greasy and pre-chilled slides and air dried. Coded Giemsa-stained slides were screened for the presence of chromosome aberrations, i.e. chromatid breaks, exchanges, intrachromatid deletions, triradials and minutes. A minimum of two experiments were conducted using three animals in each sample. The results were subjected to statistical analysis by employing the one tailed Student's t-test.
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Results |
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The data obtained from a minimum of two independent experiments are given in Tables II–IV
and their mean values are also incorporated. There were no significant variations in the frequencies of chromosomal aberrations between the two experiments (P > 0.05). Chromosomal aberrations were induced after conditioning, challenging and combined treatments of EMS after 24, 48 and 72 h RTs and their frequencies are presented in Tables II–IV. These results show that the EMS induced a very high frequency of chromatid breaks, exchanges, intrachromatid deletions and minutes at all RTs. The minutes are of chromatid-type not chromosomal-type, i.e. double minutes. The conditioning dose induced 13–15% aberrations, whereas the challenging dose produced 70–75% aberrations, which is significantly higher compared with controls (Tables II–IV and Figures 1–3). The combined treatment (conditioning-8 h TL-challenging) yielded significantly less frequencies of chromosomal aberrations compared with the respective challenge treatments at different RTs tested. These observations are compatible with the earlier experiments of the authors (Riaz Mahmood and Vasudev, 1990– 1993; Riaz Mahmood et al., 1996; Vasudev et al., 1997). The results of inter- and pretreatments of nicotinamide have revealed a significant reduction in the frequency of chromosomal aberrations (P < 0.05) compared with the combined or challenge dose (Tables II–IV and Figures 1 and 2). Nicotinamide alone induced insignificant chromosomal aberration frequencies as compared with controls. On the other hand, in the post-treatment at all time pauses, the aberration frequency was significantly reduced (P < 0.05) compared with the challenge dose, the frequency of aberrations was almost equal to the combined treatment at the 6 h time-pause. However, it is interesting to note that, at 12 or 18 h post-treatment, the reduction of chromosomal aberrations is significant compared with the combined treatment (Tables II–IV and Figure 3). Similarly, in accordance with the reduction of the frequency of chromosomal aberrations, the aberrant cell frequency was also reduced in the combined and other treatment schedules (Tables II–IV). Mitotic indices recorded show that the pre-, post- and inter-treatments of nicotinamide to the EMS-treated cells did not prolong the cell cycle (Table V).
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Discussion |
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The results of our present investigations clearly demonstrated the induction of chromosomal aberrations by EMS, which are mainly the chromatid-type of aberrations produced in the bone marrow cells of the mouse. This is in line with earlier observations, wherein the mutagenic and clastogenic effects of EMS were observed (Riaz Mahmood and Vasudev, 1990; –1994; Riaz Mahmood et al., 1996; compare with Vogel and Natarajan, 1982). Present results also point to the presence of adaptive response induced by EMS (Tables II–IV
and Figures 1–3), which is consistent with the previous reports on adaptive response induced by chemicals (Samson and Schwartz, 1980; Kaina, 1982; Olivieri and Bosi, 1990; Riaz Mahmood and Vasudev, 1990– 1993; Mudrigal-Bujaidar et al., 1994; Kleczkowska and Althaus, 1996; Nikolova and Huttner, 1996; Riaz Mahmood et al., 1996; Vasudev et al., 1997; Harish et al., 1998, 2000). Results obtained in the present investigations with 8 h TL between the conditioning and challenging were similar to the earlier observations of Riaz Mahmood and Vasudev (1993).
Wiencke (1987) who worked on the influence of PARP inhibitors on the adaptive response in in vitro human lymphocytes proposed that `ADPRT, itself and not other metabolic processes affected by inhibitors of this enzyme, plays an important role in the adaptive response'. Keeping this in mind, the present investigations were undertaken using nicotinamide as an inhibitor of PARP. The results of inter-treatment of nicotinamide (L–2 h–N–6 h–H and L–4 h–N–4 h–H) have revealed that the frequency of chromosomal aberrations has been significantly reduced compared with the combined treatment (Tables II–IV and Figure 1; P < 0.05). This indicates that the nicotinamide potentiates the EMS-induced adaptive response in the mouse bone marrow cells. In the post-treatment, as there is a significant reduction in the frequency of chromosomal aberrations at 12 or 18 h, it is proposed that nicotinamide protects the genetic system after 6 h of challenge treatment. This long duration in the activity of nicotinamide is because of the fact that the high dose of the mutagen might have disturbed the genetic machinery to release the required enzyme(s) and to repair the damage. The pre- and inter-treatment results show similarities in the way of reduction of chromosome aberrations. This may be due to the same amount of enzyme(s) released by the two different treatment schedules. This needs to be analyzed further. From the pretreatment experiments, the authors are of the opinion that nicotinamide acts as a cross-adapter by reducing the frequency of chromosomal aberrations compared with the combined treatment (Tables II–IV and Figure 2). These results are similar to that observed in the in vivo system of Poecilocerus pictus, an insect system, where the authors have demonstrated the potentiation of adaptive response by nicotinamide (Vasudev et al., 1999; Guruprasad et al., 2000). To our knowledge, these are the first reports in this direction in in vivo animal systems. Similarly, in the in vitro system of human lymphocytes, Wiencke (1987) has reported the enhancement of X-ray-induced adaptive response by nicotinamide. From the above data, it is clear that nicotinamide, an inhibitor of PARP has enhanced the adaptive response. In other words, it can be opined that PARP is not involved in the adaptive response. Furthermore, there are reports to show that the cell extracts depleted of PARP (Rhun et al., 1998) or PARP knockout mice (Wang et al., 1995) have the potency in DNA repair. Absence of PARP did not prevent DNA repair in in vitro cells (Ding et al., 1992). In support of these observations, Melissa et al. (1998) have demonstrated that there is a synthesis of poly(ADP-ribose) polymers in PARP–/– cells in a damage-dependent manner. This indicates the involvement of different mechanism(s) for the synthesis of poly(ADP-ribose) polymers in DNA repair. Caria et al. (1997) have demonstrated that there is an alternative repair pathway in the absence of PARP in in vitro human lymphocytes of the Down syndromes. Contrary to these, inhibitors of PARP increased the incidence of chromosomal aberrations, SCEs (Wiencke et al., 1986; Catena et al., 1994; Kupper et al., 1995; Schreiber et al., 1995) and suppressed the adaptive response when applied during 2 h after the adaptive treatment (Wiencke et al., 1986; Shadley and Wolff, 1987). PARP involvement in the DNA repair process was also reported in various cell types (Park and Kim, 1983; Cleaver et al., 1985; Cleaver and Morgan, 1991; Shall, 1994).
In the present studies, cytotoxicity of chemicals has been analyzed using the mitotic index of treated cells. The results of the mitotic index have shown that nicotinamide has no effect on the cell cycle and in turn enhance the mitotic divisions (Table V). This may be due to the action of nicotinamide in preserving NAD+ levels in the cells. In line with this, the nicotinamide and other inhibitors of PARP are reported to prevent depletion of NAD+ (de Murcia and Menisser de Murcia, 1994; Lindahl et al., 1995) and protect the cells from cytotoxic effects of various chemicals and drugs (Cosi et al., 1994, 1996; Cosi and Marien, 1998; Chatterjee et al., 1999; Kolb and Burkart, 1999).
In conclusion, our results have clearly indicated the potentiation of the EMS-induced adaptive response by nicotinamide in the mouse bone marrow cells (Table VI). With the data available it is not possible to highlight the actual role of PARP in the adaptive response. Further studies are required to decipher the molecular mechanism of adaptive response and the involvement of PARP in adaptive response.
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Acknowledgments |
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We wish to express our gratitude to the Professor and Chairman of the Department of Zoology for providing facilities and to the University Grants Commission for awarding the project (contract no. F.3-58/93 SR-II). K.P.G. is thankful to the CSIR, New Delhi, for the financial assistance.
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Notes |
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3 To whom correspondence should be addressed.
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Received on January 20, 2000; accepted on January 3, 2001.
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