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Fever induced in marine arthropods by prostaglandin E1
Life Sciences, 901. 25, pp . 1601-1604 Printed in the U.S .A .
Rexga~on g;ese
FEVER INDUCED IN MARINE ARTHROPODS BY PROSTAGLANDIN E1 Martha Elizabeth Caeterlin and William Wallace Reynolds The University of New Bugland,
Biddeford, Maine 04005
(Received in final form September 24, 1979)
SUMMARY Iajectiane of prostaglandin E1 into the haemocoel of the marine arthropods Limulus polyphemus, Homarue americaaus sad Penaeus duorarum induced a behaviorally mediated fever (increase in preferred temperature, resulting is increased body temperature) . The finding that PGEl is pyrogenic to arthropods as well as to mammals suggests that arthropods can be used as simple experimental models for further investigations of the aeuropharmacological role of proataglandine in fever. Lower animals, because of their relative simplicity is comparison with mammals, frequently are convenient experimental models for studies the results of which can often be applied to human biomedicine. Thermoregulatosy and febrile mechanisms are topics which are currently of great interest in biomedicine, and comparative studies can shed much light is this area . The neuropharmacological role of proetaglandins in the mediation of fever has been an area of particular interest . We have undertaken studies with aquatic and marine arthropods to determine whether prostaglandin El (PGEl) will induce fever in these animals, ae it does in mammals . Aquatic arthropods (1, 2), like other ectotherms (3), control their body temperatures by behaviorally exploiting thermal heterogeneity in their environment (4, 5) . In water, thermoregulatory behavior consists of preference and avoidance responses along thermal gradients (4, 5) . Fach apeciea has a specific preferred temperature or final thermal preferendum (4, 5) at which it will spend most of its time in a thermal gradient or similar free-choice situation. In a suitable environment, thermoregulation by behavioral means can be quite precise (6) . Fever is as increase is body temperature above normal, caused by an increase in thermoregulatoxy "set-point" induced by pyrogene (7 ). Behavioral fever (S) is an increase in preferred temperature above the normal final preferendum of the apeciea, resulting is an increased body temperature body core temperatures differ little from ambient water temperatures in (9) ; small aquatic ectotherms . Fever is generated in mammals partly by behavioral means (10), whereas in ectotherma febrile responses are entirely behavioral (B, 11) . Among the pyrogenic agents which induce fever in mammals is PG~ (10, 12) . PGE~ fever hoe been reported in an aquatic ectothermic vertebrate, tfie frog Rang esculenta (13), and in the freshwater crayfish Cambarue bartoni (14) . We report here experimental evidence for induction of fever by PGEl in three apeciea of marine arthropods . 0024-3205/79/181601-03$02,00/0 Copyright (c) 1979 Pergamon Preen Ltd
1602
PGE1 Fever in Arthropods
Vol . 25, No . 18, 1979
Methode The species tested were the American lobster äomarus americanus, the pink shrimp Penaeus duorarum, and the horseshoe "crab" Limulus polyph~us. The animals were tested individually in electronic thermoregulatory shuttleboxes which permitted them to control water and body temperatures by means of normal unconditioned locomotor movements monitored by photocells, which activated temperature-control equipment (9, 15) . After each animal reached its normothermic final preferendum (5), comparisons were made of mean preferred temperatures for 24 hours before and after injection of 0.1 mg of PGE -Na into the haemocoel (N - 10 animals of each species), or sham inj~ction of lz saline (controls, N ~ 10) . The rationale for the relatively large dosage of PG El was that the injections were not made directly into the CNS thermoregulatory control center (not . yet identified in arthropods) . The open circulatory system of these animals increased the likelihood that some PGEl would reach the CNS before being catabolized (16) . Results Preferred temperatures began to increase within minutes after injection of PGE.l-Na, and peaked within 4-8 hours at maximum amplitudes of +15°C for agme individuals of Limulua and Homarus . To preclude the possibility of circadian rhythm effects, we routinely compare mean preferred temperatures during the 24 hours before and after injection. Limulua exhibited the greatest 24-hour mean increase of +6oC (tl°C SE), while Homarua and Penaeus exhibited mean increases of +4 .7 °C and +4 .5°C (both f0 .5°C SE), respectively . All of these increases were statistically significant . Sham-injected controls showed no significant changes from the normothermic preferenda (16oC for Homarus , 27°C for Limulus , 31°C for Penaeus) . Discussion Do these findings imply that PGE i plays a normal role in thermoregulation or fever in arthropods? It is known that prostaglandins are normally ßynthesized in a number of marine invertebrates (17, 18, 19), including arthropods . PG El is known to induce fever in mammals (10, 12) and in an amphibian (13), but the role of proetaglandine in fever remains a topic of discussion which has not yet been resolved (12) . There ie evidence (20) that PGEl has a direct excitatory effect on some neurone, suggesting a possible mode of action if this occurs in the thermoregulatory control center . The finding that PGEl, ae well as bacterial endotoxin (1), induces fever in arthropods as well as in the vertebrates is not only fascinating from a comparative viewpoint, but also gives promise of a new experimental model in which to investigate the neuropharmacological mechanisms of fever . References 1. 2. 3. 4. 5. 6. 7. 8.
M . E. CASTSQLiN and W. W. REYNOLDS . Hydrobiologie 56, 99-101 (1977) . W. W. REYNOLDS and M. E. CASTERLIN. J . Thermal Biome 4, 165-166 (1979) . W. W. REYNOLDS . Amer . Zool . 19, 193-194 (1979) . W. W. REYNOLDS . J. Fish . Res:Board Can . 34, 734-739 (1977) . W. W. REYNOLDS and M. E. CASTERLIN. Amer .Zool . _19, 211-224 (1979) . W . W. REYNOLDS, M . E . CASTERLIN, and J . B . COVERT Fed. Proc . 38, 1053 (1979) . M . J . KLUGER . Amer . Zool . 19, 295-304 (1979) . W . W. REYNOLDS, M . E. CASTEi~LTN, and J . B . COVERT . Nature 259, 41-42 (1976) .
Vol . 25, No . 18, 1979
9. 10 . 11 . 12 . 13 . 14 . 15 . 16 . 17 . 18 . 19 . 20 .
PGE1 Fever in Arthropode
1603
W . W . REYNOLDS, R . W . McCAIILEY, M . E . CASTERLIN, and L . I . CRAWSHAW . Camp . Biochem . Physiol . 54A, 461-463 (1976) . L . I . CBAWSHAW and J . T .~ITT . J . Physiol . 244, 197-206 (1975) . W . W . REYNOLDS, J . B . COVERT, and M . E . CASTE~ .lN . J . Fieh Diseases 1, 271-273 (1978) . W . L . VEALE, R. E . COOPER, and Q . J . PITTMAN, in The Prostaglandins , Vol . 3, pp . 145-167, Plenum Press, New York (1977) . R . MYHRE, M . CABANAC, and G . MYHRE . Acte Physiol . Scand . 1~, 219-229 (1978) . M . E . CASTERLIN and W . W . REYNOLDS . Pharmac . Biochem . Behav . 9, 593-595 (1978) . W . W . REYNOLDS . J . Fish . Res . Boar d Can . 34 300-304 (1977) . I . BISHAI and F . COCEANI . J . Neurochem . r 2 1167-1174 (1976) . H . OGATA, T . NOMfJRA, and M . RATA . Bull . Jap . Soc . Sci . Fieh . 44, 13671370 (1978) . D . $ . MORSE, M . RAYNE, M . TIDYMAN, and S . ANDERSON . Biol . Hull . _154, 440-452 (1978) . L . Z . BITO . Comp . Biochem . Physiol . 43A, 65-82 (1972) . P . G . CAIILFORD and F . COCEANI . Can . J~Phyeiol . Pharmacol . ~ 293-300 (1977) .
Rexga~on g;ese
FEVER INDUCED IN MARINE ARTHROPODS BY PROSTAGLANDIN E1 Martha Elizabeth Caeterlin and William Wallace Reynolds The University of New Bugland,
Biddeford, Maine 04005
(Received in final form September 24, 1979)
SUMMARY Iajectiane of prostaglandin E1 into the haemocoel of the marine arthropods Limulus polyphemus, Homarue americaaus sad Penaeus duorarum induced a behaviorally mediated fever (increase in preferred temperature, resulting is increased body temperature) . The finding that PGEl is pyrogenic to arthropods as well as to mammals suggests that arthropods can be used as simple experimental models for further investigations of the aeuropharmacological role of proataglandine in fever. Lower animals, because of their relative simplicity is comparison with mammals, frequently are convenient experimental models for studies the results of which can often be applied to human biomedicine. Thermoregulatosy and febrile mechanisms are topics which are currently of great interest in biomedicine, and comparative studies can shed much light is this area . The neuropharmacological role of proetaglandins in the mediation of fever has been an area of particular interest . We have undertaken studies with aquatic and marine arthropods to determine whether prostaglandin El (PGEl) will induce fever in these animals, ae it does in mammals . Aquatic arthropods (1, 2), like other ectotherms (3), control their body temperatures by behaviorally exploiting thermal heterogeneity in their environment (4, 5) . In water, thermoregulatory behavior consists of preference and avoidance responses along thermal gradients (4, 5) . Fach apeciea has a specific preferred temperature or final thermal preferendum (4, 5) at which it will spend most of its time in a thermal gradient or similar free-choice situation. In a suitable environment, thermoregulation by behavioral means can be quite precise (6) . Fever is as increase is body temperature above normal, caused by an increase in thermoregulatoxy "set-point" induced by pyrogene (7 ). Behavioral fever (S) is an increase in preferred temperature above the normal final preferendum of the apeciea, resulting is an increased body temperature body core temperatures differ little from ambient water temperatures in (9) ; small aquatic ectotherms . Fever is generated in mammals partly by behavioral means (10), whereas in ectotherma febrile responses are entirely behavioral (B, 11) . Among the pyrogenic agents which induce fever in mammals is PG~ (10, 12) . PGE~ fever hoe been reported in an aquatic ectothermic vertebrate, tfie frog Rang esculenta (13), and in the freshwater crayfish Cambarue bartoni (14) . We report here experimental evidence for induction of fever by PGEl in three apeciea of marine arthropods . 0024-3205/79/181601-03$02,00/0 Copyright (c) 1979 Pergamon Preen Ltd
1602
PGE1 Fever in Arthropods
Vol . 25, No . 18, 1979
Methode The species tested were the American lobster äomarus americanus, the pink shrimp Penaeus duorarum, and the horseshoe "crab" Limulus polyph~us. The animals were tested individually in electronic thermoregulatory shuttleboxes which permitted them to control water and body temperatures by means of normal unconditioned locomotor movements monitored by photocells, which activated temperature-control equipment (9, 15) . After each animal reached its normothermic final preferendum (5), comparisons were made of mean preferred temperatures for 24 hours before and after injection of 0.1 mg of PGE -Na into the haemocoel (N - 10 animals of each species), or sham inj~ction of lz saline (controls, N ~ 10) . The rationale for the relatively large dosage of PG El was that the injections were not made directly into the CNS thermoregulatory control center (not . yet identified in arthropods) . The open circulatory system of these animals increased the likelihood that some PGEl would reach the CNS before being catabolized (16) . Results Preferred temperatures began to increase within minutes after injection of PGE.l-Na, and peaked within 4-8 hours at maximum amplitudes of +15°C for agme individuals of Limulua and Homarus . To preclude the possibility of circadian rhythm effects, we routinely compare mean preferred temperatures during the 24 hours before and after injection. Limulua exhibited the greatest 24-hour mean increase of +6oC (tl°C SE), while Homarua and Penaeus exhibited mean increases of +4 .7 °C and +4 .5°C (both f0 .5°C SE), respectively . All of these increases were statistically significant . Sham-injected controls showed no significant changes from the normothermic preferenda (16oC for Homarus , 27°C for Limulus , 31°C for Penaeus) . Discussion Do these findings imply that PGE i plays a normal role in thermoregulation or fever in arthropods? It is known that prostaglandins are normally ßynthesized in a number of marine invertebrates (17, 18, 19), including arthropods . PG El is known to induce fever in mammals (10, 12) and in an amphibian (13), but the role of proetaglandine in fever remains a topic of discussion which has not yet been resolved (12) . There ie evidence (20) that PGEl has a direct excitatory effect on some neurone, suggesting a possible mode of action if this occurs in the thermoregulatory control center . The finding that PGEl, ae well as bacterial endotoxin (1), induces fever in arthropods as well as in the vertebrates is not only fascinating from a comparative viewpoint, but also gives promise of a new experimental model in which to investigate the neuropharmacological mechanisms of fever . References 1. 2. 3. 4. 5. 6. 7. 8.
M . E. CASTSQLiN and W. W. REYNOLDS . Hydrobiologie 56, 99-101 (1977) . W. W. REYNOLDS and M. E. CASTERLIN. J . Thermal Biome 4, 165-166 (1979) . W. W. REYNOLDS . Amer . Zool . 19, 193-194 (1979) . W. W. REYNOLDS . J. Fish . Res:Board Can . 34, 734-739 (1977) . W. W. REYNOLDS and M. E. CASTERLIN. Amer .Zool . _19, 211-224 (1979) . W . W. REYNOLDS, M . E . CASTERLIN, and J . B . COVERT Fed. Proc . 38, 1053 (1979) . M . J . KLUGER . Amer . Zool . 19, 295-304 (1979) . W . W. REYNOLDS, M . E. CASTEi~LTN, and J . B . COVERT . Nature 259, 41-42 (1976) .
Vol . 25, No . 18, 1979
9. 10 . 11 . 12 . 13 . 14 . 15 . 16 . 17 . 18 . 19 . 20 .
PGE1 Fever in Arthropode
1603
W . W . REYNOLDS, R . W . McCAIILEY, M . E . CASTERLIN, and L . I . CRAWSHAW . Camp . Biochem . Physiol . 54A, 461-463 (1976) . L . I . CBAWSHAW and J . T .~ITT . J . Physiol . 244, 197-206 (1975) . W . W . REYNOLDS, J . B . COVERT, and M . E . CASTE~ .lN . J . Fieh Diseases 1, 271-273 (1978) . W . L . VEALE, R. E . COOPER, and Q . J . PITTMAN, in The Prostaglandins , Vol . 3, pp . 145-167, Plenum Press, New York (1977) . R . MYHRE, M . CABANAC, and G . MYHRE . Acte Physiol . Scand . 1~, 219-229 (1978) . M . E . CASTERLIN and W . W . REYNOLDS . Pharmac . Biochem . Behav . 9, 593-595 (1978) . W . W . REYNOLDS . J . Fish . Res . Boar d Can . 34 300-304 (1977) . I . BISHAI and F . COCEANI . J . Neurochem . r 2 1167-1174 (1976) . H . OGATA, T . NOMfJRA, and M . RATA . Bull . Jap . Soc . Sci . Fieh . 44, 13671370 (1978) . D . $ . MORSE, M . RAYNE, M . TIDYMAN, and S . ANDERSON . Biol . Hull . _154, 440-452 (1978) . L . Z . BITO . Comp . Biochem . Physiol . 43A, 65-82 (1972) . P . G . CAIILFORD and F . COCEANI . Can . J~Phyeiol . Pharmacol . ~ 293-300 (1977) .