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Poly Amine Metabolism During the Perinatal Development of the Rabbit Right and Left Ventricle

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Poly Amine Metabolism During the Perinatal Development of the Rabbit Right and Left Ventricle Pediatr. Res. 16: 721-727 (1982) Poly amine Metabolism during the Perinatal Development of the Rabbit Right and Left Ventricle ROBERT J. BOUCEK, JR,'"' with the Technical Assistance of ROWENA DAVIDSON Department of Pediatrics cnd Biochemistry, Vanderbilt Medical Center, Nashville, Tennessee, USA Summary cardiovascular alterations (19) is accom~aniedbv increased mvo- cardial cell number as well as increased cell sizi(l0). In the hrst The right ventricular (RV) and left ventricular (LV) free wall wk of postnatal life an increase in myocyte number accounts for weights, ornithine decarboxylase (ODC) specific activity and the 2-fold weight difference between the left and right ventricles polyamine content were determined in fetal, I-, 2-, 7-, 14, and 21- for developing rats (2). day-old rabbit hearts. There was a significant increase in the LV Other differences also have been observed in the rate of micro- free wall weight and a decrease in RV free wall weight between vascular and subcellular organelle maturation of the left versus 1-7 days. By day 7 the LV/RV mass ratio doubled and reached a right ventricle (16, 23). From the morphologic features of the ratio comparable to that seen in adult rabbit hearts. The rate of neonatal rat heart, LV growth is analogous to combined eccentric change in the LV and RV free wall weights were comparable after and concentric hypertrophy whereas right ventricular growth is day 7. analagous to eccentric hypertrophy (2). Presumably the postnatal There was a significant increase in LV ODC specific activity pressure loading of the newborn LV accelerates its rate of growth and a decrease in RV ODC specific activity after birth. The LV with features similar to concentric hypertrophy due to pressure ODC specific activity was significantly greater than RV ODC overloading in pathologic states. Thus the postnatally developing specific activity in both 1 and 2 day old rabbit hearts whereas they heart affords an ideal model for studying the relationship between were not significantly different in 7 and 14 day old rabbit hearts. pressure loading and adaptive myocardial growth because paired The molar content (nmoles/mg wet weight or nmoles/mg pro- comparisons of left and right ventricular parameters are possible. tein) of putrescine decreased approximately Ifold fter birth in the An increase in ornithine decarboxylase (EC. 4.1.1.17) activity, RV but increased approximately 2-fold in the LV. The molar and increased polyamine production by this enzyme, occurs during content of spermidine and spermine was transiently increased the initiation of adaptive myocardial growth in the pressure after birth (1 day old) in both RV and LV with approximately a 2- overloaded adult heart. Acute banding experiments have demon- fold increase in spermidine and a 2.5-fold (LV) and 4-fold (RV) strated an early rise in ornithine decarboxylase (ODC) activity increase in spermine content. The increase in LV putrescine and an increase in polyamine content in the right ventricle follow- content after birth was due, at least in part, to the observed ing pulmonary artery banding (20) and the left ventricle following increase in ODC specific activity in the LV free wall. The putres- aortic banding (4,7). This increase in ODC activity and polyamine cine/spermidine ratio increased in the LV and decreased in the synthesis has been suggested to regulate myocardial growth by the RV immediately after birth up to day 7. As opposed to the short- regulation of: (1) the synthesis of RNA (4, 5); (2) the translation lived increase in spermidine and spermine observed in both the of mRNA (9); or (3) gene expression by the polyamine regulation RV and the LV free wall, increased ODC specific activity and of the acetylation of nucleohistones (6, 15). Recently, ODC activity putrescine accumulation uniquely characterized the preferential and polyamine content have been shown to be increased in the growth of the LV between day 1 and 7. thyroxine-induced hypertrophy of the adult rat heart (17). With the use of 1,3-diam&0-2-~ro~anol,a reported inhibito; of ODC Speculation activity, the increase in polyamine content did not appear to be The postnatally developing heart affords an ideal model for essential for hype*rophy in this r~~odeland species (17). This studying the relationship between pressure loading and adaptive repod does speculate that the hypertrophy of myocardial cells, as myocardial growth because paired comparisons of left and right to hy~e~lasia*may require enhanced polyamhe ventricular parameters are possible. Age-related changes in left synthesis (17). Thus the cumulative evidence to date suggests that ventricular (LV) growth, ornithine decarboxylase (ODC) specific increased production of the polyamines and mithine decarbox- activity and putrescine accumulation occur immediately after birth ylase activity are associated with cardiac hypertrophy but their and were clearly different from the right ventricle. This increase is in LV ODC activity and putrescine synthesis may be secondary to kcau~eof the potential role of the polyamines in the regulation the alterations in hemodynamic loading of the LV in the newborn. hype~lasia (26) the age-re1ated changes in ODC If cellular hyperplasia accounts for this preferential growth of the activity and polyamine content were investigated in the left and LV in the developing rabbit heart, as has been reported to be the right ventricles of the developing rabbit heart. Because the pref- case in the developing rat heart, it is speculated that polyamine erential growth of the LV after birth is due to a higher rate of metabolism may play a role in myocardial cellular hyperplasia. cellular proliferation than the RV (2), the relationship between polyamine metabolism and myocardial hyperplasia may be ex- amined by comparing polyamine synthesis in the two ventricles. Mammalian myocardial growth after birth is characterized by The goal of this study was to determine if the initiation of the overall growth of the heart with disproportionatly greater growth physiologic growth of the LV was related to an increase in ODC of the left (or systemic) ventricle (LV) compared with the right (or activity and polyamine accumulation compared with the RV. An pulmonic) ventricle (RV) (12, 18). The rapid growth of the LV in additional goal was to determine if there was a characteristic response to the recognized postnatal hemodynamic and structural polyamine profile in the ventricle undergoing a growth response 72 1 722 BOUCEK to increased pressure loading analagous to that seen in pressure- lyophilized to dryness. After lyophilization, 0.1 ml of 0.2 N overloaded hypertrophy models (20). perchloric acid was added to the lyophilized homogenate and perchloric acid insoluble material removed by centrifugation. The MATERIALS AND METHODS polyamines extractable by perchloric acid were alkaliiized with sodium carbonate in light-shielded tubes, and 0.3 ml of a freshly Animal protocol. White New Zealand rabbits were housed and prepared 10 mg/ml dansyl chloride solution in acetone (Aldreich fed standard Purina rabbit chow and water ad libitum. Age-related Co.) was added. After an overnight reaction at room temperature, changes in body, heart, RV and LV weights, ODC specific activity unreacted dansyl chloride was removed by the addition of proline. and polyamine content was determined in rabbits 1, 2, 7, 14 and The dansyl derivatives of the polyamines were extracted with 21-days after delivery. Similar determinations were also made in toluene (3 ml x 2). A preseparation of the polyamine derivatives fetal rabbits from a litter removed surgically from a pregnant doe from other reaction products was performed (22) before high at approximately 1 day before expected partuition. All other age- performance liquid chromotgraphy. Approximately 80-90% of the related comparisons of body and heart weights, LV and RV internal standard and labeled polyamines could be dansylated and weights, ODC specific activity and polyamine content were made recovered by this method (personal observation). A filter spectro- between animals of at least two separate and comparably sized photofluorometer (Fluoro-Monitor, Aminco Co.) with a Corning litters. This protocol was adopted because removing litter mates 7-60 primary filter (355 nm), and a Wratten 2A-12 secondary filter at different ages has been shown to accelerate the rate of growth (510 nm) was used to detect the fluorescence of the dansyl of the remaining animals in the litter (10). All differences between derivatives eluted with a non-linear gradient between 45-100% right and left ventricular free wall weights, ODC specific activity, methanol. and polyamines content at each of the age points were analyzed Relative fluorescence of the dansyl derivatives in samples of as paired observations. Litters with less than five animals were authentic standards dansylated under identical conditions was not used. determined with each group of myocardial samples. Identification Tissue preparation. After rapid cervical fracture, the heart was of the putrescine, spermidine and spermine derivatives was based quickly dissected from the animal, rinsed with chilled saline to on the comigration with dansyl derivatives of authentic standards. remove all blood, blotted and weighed. The LV and RV free Each determination was corrected for internal standard recovery. walls, including the papillary muscles, were dissected free, rinsed, Statistical design. Statistical analysis of the difference in wet blotted and weighed on an analytical balance (Mettler). weight, protein and polyamine content, and ODC specific activity The RV and LV free walls were submerged in buffer at 4OC between the RV and LV was determined using a paired t test for containing: Tris-HC1 (25 mM, pH 7.4); dithiothreitol (5.0 mM); each age group. The level of significance chosen was P < 0.05. and pyridoxal-5'-phosphate (0.25 mM). The ratio of buffer volume Using linear regression analysis of the fluorescent peak areas of to tissue volume was 3.0 assuming a tissue density of 1 g/ml.
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