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Effects of Aspirin-Like Drugs on Mitogen- Stimulated DNA Synthesis of Lymphocytes from Pregnant Rats and Offspring

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Effects of Aspirin-Like Drugs on Mitogen- Stimulated DNA Synthesis of Lymphocytes from Pregnant Rats and Offspring 003 1-3998/88/2301-0093$02.00/0 PEDIATRIC RESEARCH Vol. 23, No. 1, 1988 Copyright O 1988 International Pediatric Research Foundation, Inc. Printed in U.S.A. Effects of Aspirin-Like Drugs on Mitogen- Stimulated DNA Synthesis of Lymphocytes from Pregnant Rats and Offspring RICHARD M. MILLIS, MICHAEL C. EWII, GODWIN U. OFFIAH, BARBARA P. HYDE, AND ENID M. KNIGHT Animal Physiology Laboratory, Department of Zoology, Graduate School ofArts and Sciences and Department of Human Nutrition and Food, School of Human Ecology, Howard University, Washington, D.C. 20059 ABSTRACT'. Previous studies have shown that salicylates suppression of human lymphocytes (1-4). However, results of in and protein-calorie malnutrition compromise immunologi- vivo studies of salicylates (aspirin) and suppression of lymphocyte cal responses in humans and experimental animals. The transformation have been very conflicting. present study compared the effects of prenatal normal and Crout et al. (5)found marked suppression of blastogenesis in low protein diets, with and without aspirin-like drug treat- lymphocyte transformation studies using PHA and PWM on ments, on lymphocyte blastogenesis measured by tritiated blood samples obtained from normal volunteers taking three thymidine uptake for DNA synthesis in splenic lympho- aspirin tablets (totaling 900 mg) five times daily for 4 days cytes from pregnant rats and their offspring following (therapeutic dosage). stimulation with the mitogens concanavalin A, phytohe- On the other hand, studies by Smith et al. (6) have shown that magglutinin, and pokeweedmitogen. Aspirin treatment was when 12 healthy subjects were placed on a dose of 600 mg aspirin associated with increased lvm~hocvte-- - thvmidine u~takefor five times/day for 14 days, the capability of their lymphocytes to blastogenesis in pregnant rats fed the normal protein con- incorporate [3H]thymidine in response to PHA and allogenic trol diet and their offspring. The phytohemagglutinin-stim- lymphocytes was not statistically different from that of non- ulated increase detected in offspring lymphocytes could not treated control subjects. The authors concluded that, within a 2- be statistically guaranteed. A low protein diet alone and a wk period, aspirin administered orally at therapeutic doses does normal protein diet combined with salicylamide treatment not suppress lymphocyte responsiveness to either PHA or allo- was associated with decreased blastogenesis in pregnant genic lymphocytes. Egorin et al. (7) obtained similar results in rats but not in their offspring. Salicylamide or aspirin treating human subjects with 600 or 900 mg aspirin four times combined with a low-protein diet decreased blastogenesis daily for 1 wk. They found that when taken orally, salicylate did in both dams and their offspring. Aspirin combined with a not induce any irreversible change in the capability of lympho- normal protein diet did not adversely affect blastogenesis cytes to respond to isolectin stimulation. in either pregnant rats or their offspring. This study sug- Although these results on lymphocyte reaction to mitogens are gests that low dietary protein and aspirin-like drugs may conflicting, the possibility remains that treatment with aspirin- independently decrease lymphocyte blastogenesis of preg- like drugs at a reduced dietary protein level might decrease the nant rats and in combination they may also reduce lym- immunocompetence of pregnant mothers and their offspring. phocyte blastogenesis in offspring. The significance of When used in pregnancy above pharmacological levels, aspirin- increased lymphocyte blastogenesis in both mothers and like drugs might therefore pose a risk to the fetus of mothers offspring following aspirin treatment of pregnant rats fed with poor nutritional status. a normal protein diet is unclear. (Pediatr Res 23: 93-97, Previous studies have shown that maternal protein restriction 1988) in rats retards placental and fetal growth (8). The importance of maternal dietary protein to human fetal growth and development Abbreviations has been recently underscored by directive of the U.S. Food and Drug Administration to increase the RDA of protein for pregnant PHA, phytohemagglutinin mothers. Offspring of mothers who ingest salicylates chronically PWM, pokeweed mitogen have had significantly reduced birth weights and increased peri- Con A, concanavalin A natal mortality (9). The negative nitrogen balance, uncoupling RDA, Recommended Dietary Allowance of oxidative phosphorylation, and adrenocortical activation as- HBSS, Hanks' balanced salt solution sociated with salicylate treatment (10) might produce conditions MASH, Multiple Automated Sample Harvester unfavorable to lymphocyte proliferation and antibody produc- SPSS, Statistical Package for the Social Sciences tion. The purpose of this study is to examine the interaction effect of a protein-deficient diet and aspirin-like drug ingestion during pregnancy on maternal and offspring lymphocyte transformation The results of in vitro studies on the effect of aspirin have led in response to the mitogens PHA, PWM, and Con A. some researchers to assume that aspirin ingestion leads to in vivo METHODS Received December 22, 1986; accepted September 22, 1987. Correspondence and requests for reprints Richard M. Millis, Ph.D., Assistant Professor, The Experiment I. Animals. One hundred twenty pregnant Spra- American University, 4400 Massachusetts Avenue N.W., Biology Department/ gue-Dawley rats 3 to 4 months old were used in this study. Hurst Hall 101, Washington, D.C. 2001 6. Nonpregnant weights ranged from 200 to 300 g prior to distri- 94 MILLIS ET AL. bution to cages. They were bred with normal male rats at the offspring from experiment I, group 1 were designated as group 7 Howard University Animal Resources Facility in Beltsville, MD. in experiment 11, etc. (Table 1). Diets and Food Intake. Rats were divided into six weight- Each group in experiment I1 was fed a normal control diet of matched groups of 20 rats each. Table 1 summarizes the dietary 25% protein ad libitum for 60 days. Weight gain was recorded treatments of control and experimental groups. To determine once a week. At the end of day 60, animals were sacrificed and the effects of aspirin-like drugs on an important determinant of the methods and procedures performed during experiment I were immune responses of pregnant rats and their offspring, experi- followed. mental groups of pregnant rats were fed either aspirin or salicyl- Statistical significance of differences between control and ex- amide. Animals were fed ad libitum from day 1 of gestation perimental groups was guaranteed by Duncan's multiple range through delivery (days 19-2 1). Weight gain and food intake were test computed electronically by the SPSS software program on recorded twice weekly. an IBM 270 computer. After delivery, five pups from each group were culled to each dam, and a total of 10 dams from each group was used for RESULTS weaning. The remaining 10 dams from each group were sacri- ficed by cervical dislocation and serum from blood samples was Efffcts of aspirin on Con A-stimulated lymphocytes. Aspirin collected and frozen for subsequent analysis. treatment of pregnant rats fed the normal protein control diet Mitogenic Response of Splenic Lymphocytes. Each spleen was (group 2) was associated with increased amounts of radioactive removed with sterile scissors and forceps, weighed, and trans- thymidine incorporated into DNA within lymphocytes stimu- ferred to 10 ml of cold (5" C) HBSS (Biofluid Inc., Rockville, lated by the mitogen Con A; aspirin treatment of pregnant rats MD), which was later transferred to a sterile glass Petri dish for fed the low protein diet (group 5) was associated with additional cell suspension preparation. decreases in thymidine uptake compared to animals on the Suspensions were washed twice by centrifugation with 10 cc normal protein diet both with (group 2) and without aspirin HBSS at 1500 rpm for 10 min at 5" C in a refrigerated centrifuge. treatment (group 1) (Fig. 1). The resulting pellet was suspended in 2 ml of cold culture media Similarly, Con A-stimulated lymphocytes from offspring of consisting of 9 1 % RPMI media, 4% antibiotic (250,000 U pen- dams fed aspirin with the normal protein control diet exhibited icillin/streptomycin), and 5% fetal calf serum. greater blast transformation than lymphocytes from offspring of Acetic acid (3%) was used to lyse erythrocytes and the suspen- dams fed the normal protein diet without aspirin. Lymphocytes sion was transferred to a white cell hemocytometer for counting. from the offspring of dams fed aspirin with the low-protein diet The entire cell suspension was diluted to 5 x 10' cells/ml of showed significantly less blastogenesis than lymphocytes from culture media. From this dilution, 5 x lo5 cells in 0.1 ml were offspring of dams fed aspirin with the normal protein diet and cultured in triplicate in microtiter culture dishes with either PHA less blastogenesis than lymphocytes from offspring of dams fed 0.3 13 pg in 0.1 ml; Con A 2.5 pg in 0. l ml; and PWM in a ratio the low protein diet without aspirin (Fig. 1). of 1:20 pg in 0.1 ml. Control wells with unstimulated cells Effects of aspirin on PHA-stimulated lymphocytes. When stim- contained 5 x lo6 cells in 0.1 ml culture medium. ulated by PHA, lymphocytes from pregnant dams treated with The cells were incubated for 72 h in 5% C02 atmosphere at aspirin and fed both the normal and the low protein diet (groups 37" C. Five h prior to the termination of incubation, each well 2 and 5) exhibited significantly greater blast transformation than was labeled with 1.0 @Ci[3H]thymidine (New England Nuclear, lymphocytes from pregnant dams fed the normal protein diet Boston, MA) and reincubated under the same conditions. At the without aspirin treatment (group 1) (Fig. 2). PHA-stimulated end of the incubation period, the cells were harvested via a blast transformation of lymphocytes from dams fed the low- MASH (Microbiological Associates, Walkersville, MD) onto protein diet with aspirin (group 5) was greater than that of dams MASH I1 glass fiber filters and allowed to dry overnight.
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