Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat

H. Hayashi, D. F. Nutting, K. Fujimoto, J. A. Cardelli, Dennis Black, P. Tso

Research output: Contribution to journalArticle

137 Citations (Scopus)

Abstract

Intestinal lipid absorption is associated with marked increases in the synthesis and secretion of apolipoprotein A-IV (apoA-IV) by the small intestine. Whether the increased intestinal apoA-IV synthesis and secretion results from increased fat uptake, increased cellular triglyceride (TG) content, or increased secretion of TG-rich lipoproteins by the enterocytes is unknown. Previous work from this laboratory has shown that a hydrophobic surfactant, Pluronic L-81 (L-81), is a potent inhibitor of intestinal formation of chylomicrons (CM), without reducing fat uptake or re-synthesis to TG. Furthermore, this inhibition can be reversed quickly by the cessation of L-81 infusion. Thus L-81 offers a unique opportunity to study the relationship between lymphatic TG, apoA-I and A-IV secretion. In this study, we studied the lymphatic transport of TG, apoA-I, and apoA-IV during both the inhibitory phase (L-81 infused together with lipid) and the subsequent unblocking phase (saline infusion). Two groups of lymph fistula rats were used, the control and the experimental rats. In the experimental rats, a phosphate-buffered taurocholate-stabilized emulsion containing 40 μmol [3H]triolein, 7.8 μmol of phosphatidylcholine, and 1 mg L-81 per 3 ml was infused at 3 ml/h for 8 h. This was then replaced by glucose-saline infusion for an additional 12 h. The control rats received the same lipid emulsion as the experimental rats, but without L-81 added, for 8 h. Lymph lipid was determined both by radioactivity and by glyceride-glycerol determination, and the apoA-I and apoA-IV concentrations were determined by rocket electroimmunophoresis assay. L-81 inhibited the rise in lymphatic lipid and apoA-IV output in the experimental rats after the beginning of lipid + L-81 infusion. Upon cessation of L-81 infusion, the mucosal lipid accumulated as a result of L-81 treatment was rapidly cleared into lymph as CM. This was associated with a marked increase in apoA-IV output; the maximal output was about 3 times that of the fasting level. There was a time lag of 4-5 h between the peak lymph lipid output and the peak lymph apoA-IV output during the unblocking phase in the experimental rats. There was also a comparable time lag between the maximal lipid and apoA-IV outputs in the control animals. Incorporation studies using [3H]leucine showed that apoA-IV synthesis was not stimulated during lipid + L-81 infusion, perhaps explaining the lack of increase in lymphatic A-IV secretion. Upon relief from L-81 inhibition (glucose-saline infusion), apoA-IV synthesis was markedly stimulated, which may account for the marked increase in lymph apoA-IV secretion. In both the experimental and the control rats, there was a small, but not significant, rise in the lymph apoA-I output 5-8 h after the beginning of lipid infusion. We conclude from this study that the stimulation of apoA-IV synthesis and secretion by lipid infusion is not mediated by lipid uptake into the enterocytes or cellular TG content. Rather, it is probably the events involved in the packaging and secretion of CM that are responsible for increasing apoA-IV synthesis and secretion. This study also supports findings by other investigators that acute lipid feeding has relatively little effect on lymph apoA-I synthesis and secretion.

Original languageEnglish (US)
Pages (from-to)1616-1625
Number of pages10
JournalJournal of Lipid Research
Volume31
Issue number9
StatePublished - Jan 1 1990
Externally publishedYes

Fingerprint

Lipid A
Apolipoprotein A-I
Lymph
Rats
Lipids
Triglycerides
Chylomicrons
Rat control
Enterocytes
Emulsions
apolipoprotein A-IV
Fats
Triolein
Glycerides
Glucose
Poloxamer
Taurocholic Acid
Intestinal Absorption
Radioactivity
Product Packaging

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Endocrinology
  • Cell Biology

Cite this

Hayashi, H., Nutting, D. F., Fujimoto, K., Cardelli, J. A., Black, D., & Tso, P. (1990). Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat. Journal of Lipid Research, 31(9), 1616-1625.

Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat. / Hayashi, H.; Nutting, D. F.; Fujimoto, K.; Cardelli, J. A.; Black, Dennis; Tso, P.

In: Journal of Lipid Research, Vol. 31, No. 9, 01.01.1990, p. 1616-1625.

Research output: Contribution to journalArticle

Hayashi, H, Nutting, DF, Fujimoto, K, Cardelli, JA, Black, D & Tso, P 1990, 'Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat', Journal of Lipid Research, vol. 31, no. 9, pp. 1616-1625.
Hayashi H, Nutting DF, Fujimoto K, Cardelli JA, Black D, Tso P. Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat. Journal of Lipid Research. 1990 Jan 1;31(9):1616-1625.
Hayashi, H. ; Nutting, D. F. ; Fujimoto, K. ; Cardelli, J. A. ; Black, Dennis ; Tso, P. / Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat. In: Journal of Lipid Research. 1990 ; Vol. 31, No. 9. pp. 1616-1625.
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T1 - Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat

AU - Hayashi, H.

AU - Nutting, D. F.

AU - Fujimoto, K.

AU - Cardelli, J. A.

AU - Black, Dennis

AU - Tso, P.

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N2 - Intestinal lipid absorption is associated with marked increases in the synthesis and secretion of apolipoprotein A-IV (apoA-IV) by the small intestine. Whether the increased intestinal apoA-IV synthesis and secretion results from increased fat uptake, increased cellular triglyceride (TG) content, or increased secretion of TG-rich lipoproteins by the enterocytes is unknown. Previous work from this laboratory has shown that a hydrophobic surfactant, Pluronic L-81 (L-81), is a potent inhibitor of intestinal formation of chylomicrons (CM), without reducing fat uptake or re-synthesis to TG. Furthermore, this inhibition can be reversed quickly by the cessation of L-81 infusion. Thus L-81 offers a unique opportunity to study the relationship between lymphatic TG, apoA-I and A-IV secretion. In this study, we studied the lymphatic transport of TG, apoA-I, and apoA-IV during both the inhibitory phase (L-81 infused together with lipid) and the subsequent unblocking phase (saline infusion). Two groups of lymph fistula rats were used, the control and the experimental rats. In the experimental rats, a phosphate-buffered taurocholate-stabilized emulsion containing 40 μmol [3H]triolein, 7.8 μmol of phosphatidylcholine, and 1 mg L-81 per 3 ml was infused at 3 ml/h for 8 h. This was then replaced by glucose-saline infusion for an additional 12 h. The control rats received the same lipid emulsion as the experimental rats, but without L-81 added, for 8 h. Lymph lipid was determined both by radioactivity and by glyceride-glycerol determination, and the apoA-I and apoA-IV concentrations were determined by rocket electroimmunophoresis assay. L-81 inhibited the rise in lymphatic lipid and apoA-IV output in the experimental rats after the beginning of lipid + L-81 infusion. Upon cessation of L-81 infusion, the mucosal lipid accumulated as a result of L-81 treatment was rapidly cleared into lymph as CM. This was associated with a marked increase in apoA-IV output; the maximal output was about 3 times that of the fasting level. There was a time lag of 4-5 h between the peak lymph lipid output and the peak lymph apoA-IV output during the unblocking phase in the experimental rats. There was also a comparable time lag between the maximal lipid and apoA-IV outputs in the control animals. Incorporation studies using [3H]leucine showed that apoA-IV synthesis was not stimulated during lipid + L-81 infusion, perhaps explaining the lack of increase in lymphatic A-IV secretion. Upon relief from L-81 inhibition (glucose-saline infusion), apoA-IV synthesis was markedly stimulated, which may account for the marked increase in lymph apoA-IV secretion. In both the experimental and the control rats, there was a small, but not significant, rise in the lymph apoA-I output 5-8 h after the beginning of lipid infusion. We conclude from this study that the stimulation of apoA-IV synthesis and secretion by lipid infusion is not mediated by lipid uptake into the enterocytes or cellular TG content. Rather, it is probably the events involved in the packaging and secretion of CM that are responsible for increasing apoA-IV synthesis and secretion. This study also supports findings by other investigators that acute lipid feeding has relatively little effect on lymph apoA-I synthesis and secretion.

AB - Intestinal lipid absorption is associated with marked increases in the synthesis and secretion of apolipoprotein A-IV (apoA-IV) by the small intestine. Whether the increased intestinal apoA-IV synthesis and secretion results from increased fat uptake, increased cellular triglyceride (TG) content, or increased secretion of TG-rich lipoproteins by the enterocytes is unknown. Previous work from this laboratory has shown that a hydrophobic surfactant, Pluronic L-81 (L-81), is a potent inhibitor of intestinal formation of chylomicrons (CM), without reducing fat uptake or re-synthesis to TG. Furthermore, this inhibition can be reversed quickly by the cessation of L-81 infusion. Thus L-81 offers a unique opportunity to study the relationship between lymphatic TG, apoA-I and A-IV secretion. In this study, we studied the lymphatic transport of TG, apoA-I, and apoA-IV during both the inhibitory phase (L-81 infused together with lipid) and the subsequent unblocking phase (saline infusion). Two groups of lymph fistula rats were used, the control and the experimental rats. In the experimental rats, a phosphate-buffered taurocholate-stabilized emulsion containing 40 μmol [3H]triolein, 7.8 μmol of phosphatidylcholine, and 1 mg L-81 per 3 ml was infused at 3 ml/h for 8 h. This was then replaced by glucose-saline infusion for an additional 12 h. The control rats received the same lipid emulsion as the experimental rats, but without L-81 added, for 8 h. Lymph lipid was determined both by radioactivity and by glyceride-glycerol determination, and the apoA-I and apoA-IV concentrations were determined by rocket electroimmunophoresis assay. L-81 inhibited the rise in lymphatic lipid and apoA-IV output in the experimental rats after the beginning of lipid + L-81 infusion. Upon cessation of L-81 infusion, the mucosal lipid accumulated as a result of L-81 treatment was rapidly cleared into lymph as CM. This was associated with a marked increase in apoA-IV output; the maximal output was about 3 times that of the fasting level. There was a time lag of 4-5 h between the peak lymph lipid output and the peak lymph apoA-IV output during the unblocking phase in the experimental rats. There was also a comparable time lag between the maximal lipid and apoA-IV outputs in the control animals. Incorporation studies using [3H]leucine showed that apoA-IV synthesis was not stimulated during lipid + L-81 infusion, perhaps explaining the lack of increase in lymphatic A-IV secretion. Upon relief from L-81 inhibition (glucose-saline infusion), apoA-IV synthesis was markedly stimulated, which may account for the marked increase in lymph apoA-IV secretion. In both the experimental and the control rats, there was a small, but not significant, rise in the lymph apoA-I output 5-8 h after the beginning of lipid infusion. We conclude from this study that the stimulation of apoA-IV synthesis and secretion by lipid infusion is not mediated by lipid uptake into the enterocytes or cellular TG content. Rather, it is probably the events involved in the packaging and secretion of CM that are responsible for increasing apoA-IV synthesis and secretion. This study also supports findings by other investigators that acute lipid feeding has relatively little effect on lymph apoA-I synthesis and secretion.

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