Identification of an adipose tissue-like lipoprotein lipase in perfusates of chicken liver
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1 Identifiation of an adipose tissue-like lipoprotein lipase in perfusates of hiken liver Andre Bensadoun and Tung Liu Koh Division of Nutritional Sienes and Division of Biologial Sienes, Cornel1 University, Ithaa, NY Abstrat The nature of the lipolyti ativity released from hiken livers perfused with Krebs-Ringer buffer (ph 7.) ontaining heparin (5 or 1 Ulml), fration V albumin (3%), and glyerol (2%) was investigated. The nonreirulating perfusates ontained both the previously desribed NaC1-resistant liver lipase as well as an apolp-gluativated lipoprotein lipase (LPL). Crude perfusate lipolyti ativity was separated on heparin-sepharose olumns into two enzymati peaks whih were eluted at mean NaCI molarities of.75 M (liver lipase) and 1.2 M (LPL). The liver LPL ativity was stimulated 7-fold by human apolp-glu (half maximal ativity at 1.5 Fg/ml) and inhibited by apolp-ala, apolp-ser, apolp-glni, and apolp- GlnII. Liver LPL was fully inhibited by anti-adipose LPL immunoglobulins. The liver lipase was not affeted by apolp-glu (3-34 pg/ml) or anti-adipose LPL immunoglobulins. The data demonstrate the presene in liver perfusates of a LPL with properties similar to adipose tissue lipoprotein lipase. Supplementary key words apolipoproteins Intravenous injetions of heparin in the rat, pig, and man ause release of two triaylglyerol hydrolases into the plasma. The two lipases differ in their sensitivity to NaC1, protamine sulfate, and diethyl-pnitrophenyl phosphate, and in their requirement for a lipoprotein polypeptide (1-5). One of these lipases, lipoprotein lipase (LPL, glyerol ester hydrolase, EC ) is laimed to originate solely in extrahepati tissues and requires apolp-glu for maximal ativity; the seond, resistant to high NaCl molarities and protamine sulfate, is believed to ome from the liver. In this report, evidene is presented demonstrating that hiken livers perfused with heparin-ontaining buffers release into perfusates the previously desribed NaC1-resistant liver lipase and a lipoprotein lipase that is immunologially idential to adipose tissue lipoprotein lipase. Liver perfusion MATERIALS AND METHODS Animal donors for liver perfusions were male white Leghorn hikens, 3-15 months old; they were fasted overnight before use. Animals were killed by deapitation. Following laparotomy, the right portal vein was ligated and the liver exised. Perfusion was onduted through the left portal vein with a nonreirulating buffer at a rate of 2 mllmin for a maximum period of 5 min. The perfusion solution was an avian Krebs biarbonate buffer (6) gassed with 95% C2-5% 2. To inrease the stability of the displaed lipolyti enzymes (7), the Krebs biarbonate buffer was modified by the inlusion of 2% glyerol (vlv) and 3% bovine serum albumin (fration V, Sigma Chemial Co., St. Louis, MO). In addition, the ph of the solution was adjusted to 7. at 37 C, the perfusate temperature. Heparin from porine intestinal muosa was obtained from Sigma Chemial Co. Its onentration when inluded in the perfusion fluid was either 1 or 5 U/ml. The heparin ontained 16 U/mg. Lipase assays Lipolyti ativity was assayed with a syntheti [14C]triolein substrate emulsified in the presene of gum arabi. Triolein ontaining [ l- 4Cloleate in all three positions was purhased from DHOM Produts, North Hollywood, CA. Fifty pmol of triolein was Abbreviations: LPL, lipoprotein lipase. The nomenlature of apolipoproteins employed is based on their COOH-terminal amino aids. In the terminology suggested by Alaupovi (17), they are defined as follows: apolp-ser, apoc-i; apolp-glu, apoc-11; apolp-ala, apoc-111; apolp-glni, apoa-i; apolp-glnii, apoa-11. Person to whom orrespondene and request for reprints should be addressed. 768 Journal of Lipid Researh Volume 18, 1977
2 soniated in the presene of 2 mg of gum arabi in a total volume of 2 ml with the miroprobe of a Bronwill Biosionik IV soniator. The sample was subjeted to six 15-se soniation bursts at room temperature alternating with 15-se ooling periods in ie. Two assay systems were employed to measure the two types of lipolyti ativities present in liver perfusates. The first system (low NaCl molarity, ph 8.6) ontained the following omponents in a total volume of.5 ml: 1.25 pmol of ['4C]triolein (.133 pci per pmol of triolein); 2.5 mg of gum arabi; 5 mg of albumin;.2 ml of heated rat serum;.1 mmol of Tris buffer, ph 8.6;.5 mmol of NaCl; 5 pmol of CaCI,; and -.1 ml of enzyme preparation. In the seond assay system, the NaCl molarity was 1.O M, the ph 9., and the serum was omitted. Enzyme purifiation Lipolyti ativities in liver perfusates were separated by affinity hromatography on heparin - Sepharose 4B olumns by methods previously published (7). All buffers used during purifiation ontained 3% glyerol (v/v). Pooled liver perfusates were adjusted to.3 M NaCl and 3% glyerol and were diluted suffiiently to ontain less than 8 U heparinlml before appliation to heparin -Sepharose Perfusion volume (ml) Fig. 1. Release of lipolyti ativities in avian liver perfusates. Livers exised from two 15-month-old roosters were perfused with.15 M NaCl (15 ml) and then (arrow) with modified avian Krebs biarbonate buffer ontaining 5 U heparidml. Data are presented for two representative perfusions. Conditions of assay are.1 M NaCI, serum.2 my.5 ml, ph 8.6, -; 1 M NaCI, no serum, ph 9., - ;.1 M NaCI, no serum, ph 8.6, A -A. 4 L 3 1 E \ E O w. o r.- S a 2 a 1. t I r.1 Y NoCI ph 8.6 ' 5 IO I Frot ion ( 5 ml /t u be 1 Fig. 2. Heparin-Sepharose hromatography of 15-month-old rooster liver perfusates. Liver perfusates were pooled, adjusted to a NaCl molarity of.25 M and heparin onentration of 8 Ulml and applied to a 1.5 X 15 m heparin-sepharose olumn. The olumn was developed with a linear NaCl gradient between.5 and 1.5 M NaCI in 3% glyerol,.5 M sodium barbital, ph 7., using a total volume of 26 ml. Lipolyti ativity was measured at.1 M NaCI, ph 8.6, with.2 ml of rat serum per.5 ml assay volume and at 1. M NaCI, ph 9., in the absene of serum. 4B olumns. The olumns were equilibrated with.3 M NaCl in.5 M sodium barbital buffer, ph 7.. Elution was onduted with a linear NaCl gradient from.5 to 1.5 M NaCl in.5 M sodium barbital, ph 7., using a total volume of 26 ml. NaCl molarities of samples eluted from hromatographi olumns were estimated by measuring their ondutivities (ondutivity meter, Radiometer Copenhagen). Standard urves were prepared with solutions ontaining varying molarities of NaCl in 3% glyerol (v/v),.5 M sodium barbital, ph 7.. The volume of samples assayed was alulated so that the NaCl molarity in the.5 ml assay was.1 M NaCl in the first system (.1 M NaCI, ph 8.6, Bensadoun and Koh Adipose-like lipoprotein lipase in liver perfusates 769
3 L 18 \ 16 \ 14 =-. '2 2 IO._ w ge a I.OM NoCl ph 9. by the following alternate method. Constant amounts of a given enzyme preparation were inubated with inreasing ratios of immune to ontrol immunoglobulin, the total amount of immunoglobulin protein remaining onstant. Human apolipoproteins were prepared in the laboratory of Dr. W. Virgil Brown at the University of California, San Diego, using gel filtration and diethylaminoethylellulose hromatography ( 1 1). RESULTS L ' 5 IO SO Frot ion (5 ml /tube) Fig. 3. Heparin-Sepharose hromatography of 3-month-old rooster liver perfusates. Conditions were the same as those desribed for Fig. 2. serum inluded). In this assay, sample size varied between.26 ml and.78 ml. A volume of.1 ml of enzyme solution was employed in the seond system (1 M NaCI, no serum). Other proedures Protein was determined by the proedure of Bensadoun and Weinstein (8). Anti-adipose tissue LPL sera were suessfully prepared in rabbits by methods reently published (9). Serum from a single rabbit was employed in this study. A partially purified immunoglobulin fration was prepared by five sequential preipitations in the presene of 5% ammonium sulfate at 2 C (1). The final preipitate was dissolved in.5 M ammonium biarbonate and desalted by gel filtration on Sephadex G 1. Inhibition of lipolyti ativities by this anti-lpl immunoglobulin fration was studied as follows. Constant amounts of a given enzyme preparation were inubated with inreasing amounts (- 1 pg) of anti-lpl immunoglobulins in a series of entrifuge tubes for 1 hr at 2 C. The inubation medium (.4 ml) was adjusted to.2 M NaC1, 3% glyerol, and.5 M sodium veronal buffer ph 7.. Parallel inubations were arried out with a ontrol rabbit immunoglobulin fration prepared by ammonium sulfate preipitation and gel filtration. After inubation, the tubes were entrifuged at 28,OOOg for 3 min at 4 C. Enzymati ativity in the supernatant was determined as desribed above. Inhibition of lipolyti ativities by the same partially purified immunoglobulin fration was also studied Lipolyti ativities in liver perfusates Fig. 1 presents the results of two representative liver perfusions. Lipolyti ativity was released in the perfusate when heparin was introdued in the perfusion fluid. Lipolyti ativity measured in the presene of serum and.1 M NaCl at ph 8.6 was redued to less than 25% when serum was omitted in the assay system. Similar inhibition was observed when the ativity was assayed at ph 9. in the presene of 1. M NaCI. These early results suggested that liver perfusates ontained a signifiant portion of serum-dependent, NaC1-sensitive lipolyti ativity. Heparin-Sepharose hromatography of liver perfusate lipolyti ativity Lipolyti ativity in liver perfusates was resolved by hromatography on heparin -Sepharose olumns into two learly separated peaks. Typial hromatograms and reovery of ativities are presented for two age groups, 3- and 15-month-old animals, in Figs. 2 and 3, and Table 1. Seventy to eighty perent TABLE 1. Heparin-Sepharose hromatography of pooled liver perfusates Step 3-month-old" 1 5-month-oldb pmovhr Applied Unadsorbed 487" 58' Reovered Tube Tube a Liver perfusates from six livers (3-month-old roosters) were pooled, adjusted to a NaCl molarity of.25 M and a heparin onentration of 8 U/ml and applied to a 1.5 X 15 m heparin- Sepharose olumn. Lipolyti ativity was measured at.1 M NaCI, ph 8.6, in the presene of serum (first assay system desribed in Materials and Methods). Elution profile is shown in Fig. 3. * Liver perfusates from five livers (15-month-old roosters) treated as in footnote a. Elution profile in Fig. 2. The lipolyti ativities of the unadsorbed protein frations measured at I M NaCI (seond assay systems desribed in Materials and Methods) were 125 and pmoyhr, respetively, for the liver perfusates of the 3-month-old and 15-month-old roosters. 77 Journal of Lipid Researh Volume 18, 1977
4 of the applied ativity was retained on the olumns. Elution of the heparin -Sepharose olumns with a NaCl gradient yielded two learly resolved ativity peaks. The first peak was eluted at.75 M NaCl. Its enzymati ativity was not inhibited by 1 M NaCl; 3 1 frations in the asending portion of the first peak from five purifiations gave a mean reovery of ativity in the presene of 1 M NaCl of % (relative to ativity at.1 M NaCl). In ontrast, the seond peak, eluted at 1.15 M NaCl, was essentially inhibited when assayed at ph 9. in the presene of 1. M NaCl; 19 frations from four purifiations NoCI-RESISTANT LIPASE sampled in the desending portion of the seond peak yielded a mean reovery of %. In all purifiations performed, the sum of reovered ativities in the first and seond peaks was higher than that adsorbed to affinity olumns, suggesting that the rude perfusates ontained lipase inhibitors. The adsorbed ativity is defined as the ativity applied on the olumn minus the unadsorbed ativity. In the two purifiations summarized in Table 1, the reoveries of enzyme ativities were 13 and 12% (relative to adsorbed ativities), respetively, for liver perfusates of 3- and 15-month-old roosters. LIVER LPL apolp-ala (pa/ml) apolp-gln II (pglml) apo Lp-Gln IL (ug/ml) Fig. 4. Effet of apolp-ala, apolp-ser, apolp-glni and apolp-glnii on NaC1-resistant liver lipase and liver lipoprotein lipase. Enzyme preparations employed were those obtained by heparin- Sepharose hromatography. For the liver LPL studies the apolipoproteins were added to omplete assay systems ontaining.2 ml of rat serum,.1 M NaCI,.2 M Tris buffer, ph 8.6. In the experiments with the NaC1-resistant liver lipase, serum was omitted and the assays were onduted in the presene of 1. M NaCI,.2 M Tris buffer, ph 9.. Enzyme ativities are expressed as perentages of that present in the Tbsene of the apolipoprotein of interest. Enzyme preparations employed had the following ativities: NaC1-resistant lipase, 4.2 pmoyml per hr; liver LPL, 3.97 pmovml per hr. The enzyme volumes employed for eah assay tube were.1 and.4 ml, respetively, for the NaC1-resistant lipase and the liver LPL. Bensadoun and Koh Adipose-like lipoprotein lipase in liver perfusates 771
5 - NaCI-RESISTANT LIPASE LIVER LPL z 7 : 5 1 w o apolp-glu (ug/ml) opolp-glu (ug/ml) Fig. 5. Effet of apolp-glu on NaC1-resistant liver lipase and liver lipoprotein lipase. Conditions are the same as those outlined in Fig. 4 exept that serum was omitted in the assay of the liver LPL. Enzyme preparations employed had the following ativities in the absene of apolp-glu: NaCl resistant lipase, 9.2 pmoyml per hr; liver LPL,.366 pmollml per hr. The enzyme volume employed for eah assay tube was.4 ml for both lipases. Charaterization of two lipolyti enzymes in liver perfusates Figs. 1 and 2 illustrate the differenes in sensitivity to NaCl of the first and seond peaks. On the basis of this property and the NaCl molarities at whih these two ativity peaks were eluted, it beame apparent that the first peak was very similar to the previously desribed liver lipase and the seond ativity 12r o n n NoCl-resisioni lipose ::I,\..., ~ *, IO Anti-Adipose LPL Ig (pg/ inubation) Fig. 6. Effet of an anti-adipose LPL immunoglobulin on NaCI-resistant lipase and liver LPL. Constant amounts of enzyme (NaCI-resistant lipase,.69 ml,.462 pmol/ml per hr; liver LPL,.12 ml,.262 pmouml per hr) were inubated in entrifugal tubes for 1 hr at 2 C with inreasing amounts of rabbit antiadipose LPL immunoglobulin or ontrol rabbit immunoglobulin in a total inubation volume of.4 ml. After inubation, the tubes were entrifuged at 28,OOOg for 3 min at 4 C. Enzymati ativities in.2 ml of the supernatants were determined in the presene of.1 M NaCl for LPL and 1. M NaCl for the liver lipase. Ativity measured in the presene of immune immunoglobulin was expressed as a perentage of that present in the presene of ontrol immunoglobulin. TABLE 2. Effet of age on lipolyti ativity of liver perfusates Total Lipolyti Liver Ativity at 1. M NaCl x lob Age Ativity" Weight Ativity at.1 M NaCl months 2. (6) 2.5 (13) 3. (12) 4. (3) 5.5 (9) 15. (8) 22. (4) pmollhr 138 f ?.6' 31 f I79 f r f a 1.2 g % 77% f a Total lipolyti ativity represents the lipolyti ativity measured at.1 M NaCI, ph 8.6, in the perfusate of a single liver. Perfusion buffer ontained 1 Ulml heparin. Perfusion volume was limited arbitrarily to 1 ml. Numbers of livers perfused are indiated in parentheses. Results are means 5 standard errors. Lipolyti ativity measured in the presene of 1 M NaCl expressed as a perentage of that measured in the presene of.1 M NaCI. Mean f standard errors of seven livers. peak to the adipose tissue LPL. This provisional identifiation was onfirmed by studying the effets of human apolipoproteins on these two partially purified lipolyti ativities. ApoLp-Ala, apolp-ser, apolp-glni, and apolp-glnii inhibited both ativities (Fig. 4); apolp-glu stimulated the LPL and had no effet on the liver lipase (Fig. 5). The ph optimum of the liver LPL measured with Tris buffers (.2 M in the assay) was 9.. A partially purified immunoglobulin fration prepared from anti-adipose tissue LPL sera inhibited the liver LPL ativity but did not alter the liver lipase. Similar results were obtained when inreasing amounts of anti-lpl immunoglobulins were inubated with onstant amounts of enzyme (Fig. 6) and when the amount of immunoglobulins (immune plus ontrol) was maintained onstant during preinubation (data not shown). Effet of age on liver lipolyti ativity Age had a marked effet on both the total lipolyti ativity and the ratio of the two lipolyti ativities in liver perfusates. In mature animals (15 months and older) total lipolyti ativity appearing in 1 ml of perfusate was lower than in the young animals (2-5 months) studied (Table 2). These differenes are further aentuated when the data are expressed per g of liver weight. Assay of the lipolyti ativity in the presene of 1 M NaCl suggests that the liver lipoprotein lipase is a minor omponent in the perfusate of young roosters but aounts for most of the lipolyti ativity in the mature animals. These effets of age were also onfirmed when the two lipolyti ativities were resolved by hromatography on heparin-sepharose olumns (see Figs. 2 and 3). 772 Journal of Lipid Researh Volume 18, 1977
6 DISCUSSION This study douments the presene in the rooster liver perfusates of two distint lipolyti enzymes. One of these resembles the previously desribed NaClresistant liver lipase (1-3); the seond exhibits properties similar to those of avian adipose tissue LPL (9). The two lipolyti ativities were learly resolved by hromatography on heparin-sepharose 4B olumns. The identifiation of the seond ativity peak as a lipoprotein lipase was established by its stimulation by apolp-glu and its inhibition by 1 M NaCl and speifi anti-adipose LPL immunoglobulins. Liver LPL has been deteted immunologially by Yasuoka and Fujii (12) in the rat. The antiserum employed was prepared against postheparin rat LPL prepared by the method of Fielding (13). Their data indiate that, in 15-2 g rats, approximately half of the lipolyti ativity extrated from fresh livers with.67 M phosphate buffer at ph 7.4 is a lipase immunologially idential to plasma LPL. Ganesan, Ganesan, and Bradford (14) have reported the presene in dog liver perfusates of a C-I (apolp-ser)- ativated lipoprotein Iipase. This lipolyti ativity was not stimulated by C-I1 (apolp-glu). Failure to identify suh a lipolyti ativity in avian liver perfusates may reflet speies or experimental differenes. Kelley et al. (15) have reported that the avian hepati NaC1-resistant lipase released by heparin in the plasma dereased in females with egg laying or in males injeted with diethylstilbestrol. In the present study with male hikens a dramati derease in saltresistant liver lipase was observed with age. The hormonal status of these animals was not determined and it is therefore not possible to orrelate this derease with speifi alterations in hormone titers. The site of synthesis as well as the funtional roles of the liver LPL and of the salt-resistant liver lipase are still unknown. Both enzymes may at in onert in the transfer of remnant triglyeride fatty aids into the parenhymal ells. Alternatively, the liver LPL might represent enzyme protein originating in extrahepati tissues. The identifiation in the liver of a LPL immunologially idential to adipose tissue LPL is onsistent with the theory of Felts, Itakura, and Crane (16) that LPL assoiated with VLDL and hylomiron remnants is taken up by the 1iver.m This work was supported by U.S. Publi Health Servie Grant HL Manusript reeived 25 Apt and aepted 21 July REFERENCES 1. LaRosa, J. L., R. I. Levy, H. G. Windmueller, and D. S. Fredrikson Comparison of the triglyeride lipase of liver, adipose tissue, and postheparin plasma, J. Lipid Res. 13: Krauss, R. M., H. G. Windmueller, R. I. Levy, and D. S. Fredrikson Seletive measurement of two different triglyeride lipase ativities in rat postheparin plasma. J. Lipid Res. 14: Ehnholm, C., H. Greten, and W. V. Brown A omparative study of post-heparin lipolyti ativity and a purified human plasma triaylglyerol lipase. Biohzm. Biophys. Ata. 36: Jansen, H., and W. C. Hulsmann Liver and extrahepati ontributions to postheparin serum lipase ativity of the rat. Biohim. Biophys. Ata. 369: Fielding, C. J Further haraterization of lipoprotein lipase and hepati post-heparin lipase from rat plasma. Biohim. Biophys. Ata. 28: Benzinkert, K., and H. A. Krebs Physiologial saline for birds. Klin. Wohenshr. 12: Bensadoun, A., C. Ehnholm, D. Steinberg, and W. V. Brown Purifiation and haraterization of lipoprotein lipase from pig adipose tissue. J. Biol. Chm. 249: Bensadoun, A., and D. Weinstein Assay of proteins in the presene of interfering materials. Anal. Biohem. 7: Kompiang, I. P., A. Bensadoun, and M. W. W. Yang Effet of an antilipoprotein lipase serum on plasma triglyeride removal. J. Lipid Res. 17: Williams, C. A,, and M. W. Chase Methods in Immunology and Immunohemistry. Aademi Press, New York, NY. 1: Brown, W. V., R. I. Levy, and D. S. Fredrikson Further separation of the apoproteins of the human plasma very low density lipoproteins. Biohim. Biophys. Ata. 2: Yasuoka, S., and S. Fujii Relationship between learing fator lipase and lipases in tissues. J. Biohem. 7: Fielding, C. J Purifiation of lipoprotein lipase from rat postheparin plasma. Biohim. Biophys. Ata. 178: Ganesan, G., D. Ganesan, and R. H. Bradford Charaterization of a triglyeride hydrolase sereted by anine liver maintained in vitro. Pro. SOC. Exp. Baol. Med. 151: Kelley, J. L., D. Ganesan, H. B. Bass, R. H. Thayer, and P. Alaupovi Effet of estrogen on triaylglyerol metabolism: Inhibition of post-heparin plasma lipoprotein lipase by phosvitin, an estrogen indued protein. FEBS Lett. 67: Felts, J. M., H. Itakura, and R. T. Crane The mehanism of assimilation of onstituents of hylomirons, very low density lipoproteins and remnants. A new theory. Biohem. Biophys. Res. Commun. 66: Alaupovi, P Apolipoproteins and lipoproteins. Atheroslerosis. 13: Bemadoun and Koh Adipose-like lipoprotein lipase in liver perfusates 773
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