Effect of protein malnutrition on the metabolism of uteral collagen in the rat*
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1 J. Biosci., Vol. 3, Number 4, December 1981, pp Printed in India. Effect of protein malnutrition on the metabolism of uteral collagen in the rat* J. SAMBASIVA RAO and V. H. RAO** Biochemistry Laboratory, Central Leather Research Institute, Madras MS received 8 August 1980; revised 18 July 1981 Abstract. Protein malnutrition in the rat resulted in a reduction in the syntehsis of collagen as determined by changes in the specific and total radioactivity incorporated following a single injection of [ 3 H]-proline. It was also accompanied by a retardation in the maturation of soluble to insoluble collagen. In addition, protein deficiency was accompanied by decreased rates of catabolism of both soluble and insoluble collagen. Keywords. Collagen metabolism; uterus; protein-malnutrition. Introduction Protein malnutrition results in decreased tensile strength of wounds, tail tendons and skin in rats (Peacock, 1960) as well as impaired wound healing both in human and experimental animals (Edwards & Dumphy, 1958; Peacock, 1961; Stahl, 1963a; b). The results of a number of studies indicated that the level of protein in the diet had an effect on collagen metabolism. The collagen content and its synthesis were decreased in rats fed on a protein-deficient diet (Dickerson and John, 1969; Rao and Bose, 1969; Anasuya and Rao, 1970; McClain and Wiley. 1975; Angeleli et al. 1978; Arumugam and Bose, 1979). Previous isotopic studies in this laboratory suggested a decrease in the metabolism of dermal collagen in protein deficient animals compared to controls (Rao and Rao, 1980a). The urinary excretion of hydroxyproline as well as hydroxylysylglyco sides postulated to reflect the turnover of body collagen was decreased in protein malnutrition indicating that the metabolism of collagen was adversely affected (Whitehead, 1965; Rao and Bose. 1969: Anasuya and Rao, 1970; Rao and Rao, 1980b). * Presented at the Symposium of the Society of Biological Chemists, India, held at Lucknow in October, ** Present address: Division of Metabolism, Department of Pediatrics, University of Zurich. Kinderspital, Steinwiesstrasse 75, CH-8032, Switzerland. To whom requests for reprints should be addressed. 449
2 450 Rao and Rao In the present investigation, incorporation of [ 3 H]-proline was used as an indicator of the synthesis as well as maturation of collagen and the catabolism of both the soluble and the insoluble collagen fractions in the uterus of normal and protein malnourished albino rats was studied. Materials and methods Twenty one day old weanling female albino rats were fed a basal diet for one week and then divided into two groups. The first group continued on the basal diet (control) and the second group was fed a low protein diet, described in table 1. The control rats were pair-fed with protein-deficient animals to compensate for the decreased food intake in the protein deficient animals (Rao and Bose, 1969). Water was freely available. Daily records of food consumption were kept and body weights were taken every week. Table 1. Composition of different diets. * Salt mixture used had the following composition (in g) NaCl,105; KCl, 120; ΚΗ 2ΡΟ 4,310; Ca 3 (PO 4 ) 2,149; CaCO 3,210; MnSO 4 (anhydrous), 0.20; K 2 A1 2 (SO 4 ) 4 24 H 2 O,0.09; MnSO 4 (anhydrous),90; FePO 4.4H 2 O,14.7; CuSO 4.5 H 2 O,0.39; NaF, 0.57; KI,0.05. In addition the following three elements were also added (mg/kg diet) ZnCl 2,1.5 and CoCl 2 6 H 2 O,0.15. ** The vitamin mixture contained (mg/100g diet) thiamine hydrochloride. 0.8; riboflavin,0.8; pyridoxine hydrochloride, 0.6; niacin 5; calcium pantothenate 4; inositol, 20; choline chloride 200; folic acid 0.4, vitamin B 12, 2.0 µg; biotin, 20 µg; vitamin A acetate, 1000 I.U; vitamin D,150 I.U; α-tocoferol,12 mg and menadione,0.3 mg. On the 23rd day, subgroups of control and protein-deficient animals were injected 30 µci of [ 3 H]-proline per 100 g body weight, intraperitoneally [proline- T(G) sp. act. 1,500 mci/mmol., obtained from BARC, Bombay]. Urine was collected under toluene for a period of 12 h after the administration of labelled proline. At intervals of 12 and 120 h, the animals were killed and uteri removed immediately for processing. The remaining animals in both the groups received 50 µci of [ 3 H]-proline per 100 g body weight intraperitoneally at the start of the experiment i.e. day 1. On day 28, urine was collected under toluene for a period of 24 h. Analysis of uterus The uteri were freed from the adhering tissues and the samples were homogenized. For the convenience of analysis, three uteri from each group were pooled together to make one sample thus making six samples in each group.
3 Collagen metabolism in protein malnutrition 451 The minced material was extracted thrice with 0.45 Μ NaCl (ph 7.4) at 4 C for 24 h with one drop of octan-2-ol added as a preservative (Levene and Gross, 1959). An aliquot of the combined extracts containing the neutral salt-soluble collagen was hydrolyzed with an equal volume of 12 Ν HCl at 110 C for 24 h. The residue left after NaCl extraction, consisting of insoluble collagen was also similarly hydrolyzed. In the hydrolysates of both salt soluble and insoluble collagen, the hydroxylproline content, as well as the radioactivity of [ 3 H]-hydroxyproline was determined by the method of Rojkind and Gonzalez (1974). The collagen content was calculated by multiplying the hydroxyproline content by 7.46 (Neuman and Logan, 1950). The radioactivity was measured in an automated liquid scintillation spectrometer (Model LSS 34, Electronic Corporation of India Ltd., Hyderabad). The counting efficiency was 31% for tritium. Analysis of urine After hydrolyzing the peptides in the urine samples, the content and the radioactivity of hydroxyproline were determined as mentioned earlier. Statistical methods The results were statistically evaluated using Student's 't' test. The differences were regarded as significant at the level of P<0.05. Results The mean body weight of the control animals progressively increased from an initial value of 50 g to 92 g, after 28 days. The growth rate of the animals on the proteindeficient diet was found to be slower than that of control animals and reached a weight of 72 g after 28 days. The differences in the weight gain between the two groups are significant from the second week onwards and upto the end of the experiment. Synthesis of collagen To study the influence of protein malnutrition on the synthesis of collagen, the amount of incorporation of [ 3 H]-proline as [ 3 H]-hydroxyproline into the neutral salt-soluble collagen fraction of the uterus was examined at 12 and 120 h after the administration of labelled proline. This fraction, which contains the most recently synthesized collagen as well as some slightly older soluble collagen was found to be labelled maximally within 24 h after the injection of the isotope (Jackson and Bentley, 1960). The proportion of soluble collagen (calculated in relation to 100 mg of total collagen content in the uterus) in the protein-deficient animals was considerably lower than in the controls (table 2). The specific and total radioactivities of [ 3 H]-hydroxyproline in the protein-deficient animals at 12 and 120 h after the injection of [ 3 H]-proline were also significantly decreased as compared to controls (table 2).
4 452 Rao and Rao Table 2. Effect of protein malnutrition on the yield of neutral salt-soluble collagen (NSC) and on the specific and total radioactivity of [ 3 H] -hydroxyproline into this fraction of uterus*. * Values are mean ± SEM. ** Significant at p<0.05 a Expressed as mg/100mg collagen b Expressed as dpm/µg hydroxyproline c Expressed as dpm/100 mg collagen Conversion of soluble to insoluble collagen Table 3 shows the yield of insoluble collagen in terms of the specific and total radioactivities of insoluble collagen at 12 and 120 h after the injection of labelled proline. Both the specific and total radioactivities of [ 3 H]-hydroxyproline in the insoluble collagen were decreased considerably in the protein-deficient animals as compared to controls. Table 3. Effect of proiein-malnutrition on the yield of insoluble collagen (INC) and on the specific activity of [ 3 Ή]-hydroxyproline in the INC of uterus* * Values are mean ± SEM ** Significant at p<0.05 a Expressed as mg/100 mg collagen. b Expressed as dpm/µg hydroxyproline c Expressed as dpm/100 mg collagen. When the total radioactivity of the soluble and the insoluble collagen was expressed as a percentage of the sum of both (table 4), 75% of the activity was present in the soluble collagen and 25% in the insoluble collagen in the control
5 Collagen metabolism in protein malnutrition 453 animals, 12 h after the injection of [ 3 H]-proline. The corresponding values for protein-deficient group were 80 and 20% respectively. After 120 h, 16% of the radioactivity was present in the soluble collagen and 84% in the insoluble collagen in controls, whereas the deficient group showed 23% in the soluble collagen and 77% in the insoluble collagen. Table 4. Efect of protein malnutrition on the conversion of soluble collagen to insoluble collagen* * Data calculated from tables 2 and 3. a The total activity of 3 H -hydroxyproline in soluble and insoluble collagen is expressed in terms of percentage of the sum of both. Catabolism of soluble collagen The catabolism of soluble collagen was studied by measuring the urinary excretion of [ 3 H]-hydroxyproline during the first 12 h after [ 3 H-proline injection. The urinary excretion of hydroxyproline and the specific radioactivity of [ 3 H]-hydroxyproline in the urine of protein-deficient animals were about two thirds of that in the controls (table 5). The total radioactivity of [ 3 H]-hydroxyproline was also decreased to a great extent (about 52%). Comparison of the total radioactivity of [ 3 H] -hydroxyproline in urine with that of the soluble fraction of collagen in the uterus of protein-deficient animals showed that the total radioactivity of [ 3 H]- hydroxyproline in urine (52%, table 5) was greater than in that of the soluble collagen (36%, table 2). Table 5. Efect of protein-malnutrition on the urinary excretion of hydroxyproline and on the specific and total radioactivity of [ 3 H]-hydroxyproline during first 12 h after [ 3 H]-proline administration*. * Values are mean ± SEM a Expressed as µg/12 h. ** Significant at P<0.05. b Expressed as dpm/µg hydroxyproline. c Expressed as dpm.
6 454 Rao and Rao Catabolism of insoluble collagen Urine was collected for 24 h on the 28th day after the administration of [ 3 H]-proline. The urinary excretion of hydroxyproline was about 56% of that in the controls (table 6). Evertthough both the groups exhibited similar specific radioactivity, the total activity of [ 3 H] -hydroxyproline in the deficient rats was only 70% of that in the controls. Table 6. Effect of protein malnutrition on the urinary excretion of hydroxyproline and on the specific radioactivity and total radioactivity of [ 3 H]-hydroxyproline* * Values are mean ± SEM, a Expressed as µg/24 h. ** Significant at p<0.05 b Expressed ad dpm/µg hydroxyproline. *** Not significant. c Expressed as dpm. Discussion Measurement of [ 3 H]-hydroxyproline after the injection of labelled proline in individual fractions of uterus collagen as well as its urinary excretion gives valuable information on the metabolic turnover of collagen, its synthesis, the conversion of soluble to insoluble collagen and the catabolism of both soluble and insoluble fraction. The synthesis of collagen can be studied by following the radioactivity of [ 3 H] -hydroxyproline in soluble collagen within the first few hours and days after the injection of labelled proline. It has been reported (Prockop, 1964) that in young rats, about two thirds of the urinary hydroxyproline is derived from the insoluble collagen and about one third from the soluble collagen fraction. It is therefore, possible to study the catabolism of both soluble and insoluble collagen fractions by measuring urinary [ 3 H] -hydroxyproline 12 h and 4 weeks respectively, after the administration of labelled proline. The amount of [ 3 H]-hydroxyproline measured in soluble and insoluble collagen at 12 and 120 h yields information about the conversion of soluble to insoluble collagen. Eventhough soluble collagen represents mainly newly synthesized collagen (Jackson and Bentley, 1960), the degradation of insoluble collagen may also contribute to the amount of soluble collagen (Prockop and Kivirikko, 1968). Thus, the decrease in the content of soluble collagen in the uteri of proteindeficient animals is in accordance with decreased collagen synthesis as well as inhibited degradation of insoluble collagen. In the present investigation, the specific activity of hydroxyproline in the soluble collagen was decreased by about 18% while the total activity was more markedly decreased (about 36%) due to the influence of protein malnutrition (table 2).
7 Collagen metabolism in protein malnutrition 455 These results therefore suggest that collagen synthesis is decreased in proteindeficient animals. The lowered excretion of urinary hydroxyproline in protein-deficient animals (table 5 and 6) may be due to either decreased synthesis or decreased catabolism of collagen or both (Kivirikko, 1970). A diminished urinary excretion of hydroxylproline as well as of hydroxylysyl glycosides has also been reported in protein malnutrition (Whithead, 1965; Picou et al., 1965; Widdowson and Whitehead, 1966; Anasuya and Rao, 1966; Rao and Bose, 1969; Anasuya and Rao, 1970; Rao and Rao, 1980b). The decreased total radioactivity of hydroxyproline in both uterine soluble collagen (table 2) and the urine (table 5) may be partly explained by decreased collagen synthesis. The total radioactivity of [ 3 H]-hydroxyproline was decreased more than the total radioactivity of [ 3 H]-hydroxyproline in the uterine soluble collagen. These results may therefore indicate decreased synthesis and catabolism of soluble collagen. The results of the present investigation further suggest a decrease in the catabolism of insoluble collagen since the total radioactivity of urinary [ 3 H]-hydroxyproline measured 4 weeks after the administration of labelled proline was considerably lower in the protein-deficient animals. The radioactivity of [ 3 H]-hydroxyproline in soluble and insoluble collagen measured at 12 and 120 h after the administration of labelled proline (table 2 and 3) also suggests an impaired conversion of soluble to mature, insoluble collagen in protein malnutrition. These results therefore, collectively indicate that the synthesis of collagen, catabolism of both soluble and insoluble collagen and the maturation of uterine collagen are decreased in protein-deficient animals, compared to controls. Acknowledgements The authors are thankful to Prof. M. Santappa, Director for his keen interest and permission to publish this work. The financial assistance to one of the authors (J.S.R.) by the Council of Scientific and Industrial Research, New Delhi is gratefully acknowledged. References Anasuya, A. and Rao, B. S. N. (1966) Indian J. Med. Res., 54, 849. Anasuya, A. and Rao, Β. S. Ν. (1970) Brit. J. Nutr., 24, 97. Angeleli, A. Y. O., Burini, R. C. and Compana, A. O. (1978) J. Nutr., 108, Arumugham, R. and Bose, S. M. (1979) Acta Biochem. Pol., 26, 295 Dickerson, J. W. T. and John, P. M. V. (1969) Brit. J. Nutr., 23, 917. Edwards, L. C. and Dumphy, J. Ε. (1968) New Engl. J. Med., 259, 275. Jackson, D. S. and Bentley, J. P. (1960) J. Biophys. Biochem. Cytol., 7, 37. Kivirikko, K. I. (1970) Int. Rev. Conn. Tiss. Res., 5, 93. Levene, C, I. and Gross, J. (1950) J. Exp. Med., 110, 771. McClain, P. E. and Wiley, Ε. R. (1976) Nutr. Rep. Int., 12, 317. Neuman, R. E. and Logan, Μ. Α. (1960) J. Biol. Chem., 186, 649. Peacock, Ε. Ε. (1960) Proc. Soc. Exp. Biol. Med., 105, 380. Peacock, Ε. Ε. (1961) Surg. Gynec. Obstet., 113, 329. Picou, D., Alleyne, G. A. O. and Sea King, Α. (1966) Clin. Sci., 29, 517. Prockop, D. J. (1964) J. Clin. Invest., 43, 463.
8 456 Rao and Rao Prockop, D. J, and Kivirikko, Κ. I. (1968) Treatise on collagen, ed. D. S. Gould (London: Academic Press) A2, 216. Rao, J. S. and Rao, V. H. (1980a) Ital. J. Biochem., 29, 1. Rao, J. S. and Rao, V. H. (1980b) J. Clin. Chem; Clin. Biochem., 18, 287. Rao, V. H. and Bose, S. M. (1969) Biological aspects of leather manufacture, eds R. Bhakaran, S. C Nandy and V, S. Krishnamurthi (Central Leather Research Institute), pp Rojkind, ML and Gonzalez, E. (1974) Anal. Biochem., 57, 1. Stahl, S. S. (1963a) J. Dent. Res., 42, Stahl, S. S. (1963b) Arch. Oral. Biol., 7, 661. Widdowson, E. M. and Whitehead, J. Μ. L. (1966) Nature (London), 212, 683. Whitehead, R. G. (1966) Lancet, 1, 667.
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