Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents.
Glucagon-like peptide-1 (GLP-1) and peptide YY (PYY) are anti-diabetes/obesity hormones secreted from the gut after meal ingestion. We have shown that dietary-resistant starch (RS) increased GLP-1 and PYY secretion, but the mechanism remains unknown. RS is a fermentable fiber that lowers the glycemic index of the diet and liberates short-chain fatty acids (SCFAs) through fermentation in the gut. This study investigates the two possible mechanisms by which RS stimulates GLP-1 and PYY secretion: the effect of a meal or glycemic index, and the effect of fermentation. Because GLP-1 and PYY secretions are stimulated by nutrient availability in the gut, the timing of blood sample collections could influence the outcome when two diets with different glycemic indexes are compared. Thus we examined GLP-1 and PYY plasma levels at various time points over a 24-h period in RS-fed rats. In addition, we tested proglucagon (a precursor to GLP-1) and PYY gene expression patterns in specific areas of the gut of RS-fed rats and in an enteroendocrine cell line following exposure to SCFAs in vitro. Our findings are as follows. 1) RS stimulates GLP-1 and PYY secretion in a substantial day-long manner, independent of meal effect or changes in dietary glycemia. 2) Fermentation and the liberation of SCFAs in the lower gut are associated with increased proglucagon and PYY gene expression. 3) Glucose tolerance, an indicator of increased active forms of GLP-1 and PYY, was improved in RS-fed diabetic mice. We conclude that fermentation of RS is most likely the primary mechanism for increased endogenous secretions of total GLP-1 and PYY in rodents. Thus any factor that affects fermentation should be considered when dietary fermentable fiber is used to stimulate GLP-1 and PYY secretion.
Zhou
June
J
Pennington Biomedical Research Center, Baton Rouge, LA 70808, USA. zhouj@pbrc.edu
Martin
Roy J
RJ
Tulley
Richard T
RT
Raggio
Anne M
AM
McCutcheon
Kathleen L
KL
Shen
Li
L
Danna
Samuel Colby
SC
Tripathy
Sasmita
S
Hegsted
Maren
M
Keenan
Michael J
MJ
D000273:Adipose Tissue / Q000187:drug effects / Q000378:metabolism; D000818:Animals; D001786:Blood Glucose / Q000378:metabolism; D002460:Cell Line; D002766:Cholecystokinin / Q000235:genetics; D004040:Dietary Carbohydrates / Q000008:administration & dosage / Q000378:metabolism / Q000494:pharmacology*; D018819:Dipeptidyl Peptidase 4 / Q000097:blood; D004435:Eating / Q000187:drug effects; D005260:Female; D005285:Fermentation; D005753:Gastric Mucosa / Q000378:metabolism; D015870:Gene Expression / Q000187:drug effects; D054439:Ghrelin / Q000235:genetics; D052216:Glucagon-Like Peptide 1 / Q000097:blood*; D006801:Humans; D007328:Insulin / Q000097:blood; D007413:Intestinal Mucosa / Q000378:metabolism; D007422:Intestines / Q000187:drug effects; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D019894:Peptide YY / Q000097:blood* / Q000235:genetics; D052336:Proglucagon / Q000235:genetics; D051381:Rats; D017207:Rats, Sprague-Dawley; D013213:Starch / Q000008:administration & dosage / Q000378:metabolism / Q000494:pharmacology; D013270:Stomach / Q000187:drug effects
D001786:Blood Glucose; D004040:Dietary Carbohydrates; D054439:Ghrelin; D007328:Insulin; D019894:Peptide YY; D052336:Proglucagon; D052216:Glucagon-Like Peptide 1; D013213:Starch; D002766:Cholecystokinin; D018819:Dipeptidyl Peptidase 4
Can J Physiol Pharmacol. 1985 Sep;63(9):1113-21
2413977
J Clin Invest. 1996 Apr 1;97(7):1767-73
8601643
Obesity (Silver Spring). 2006 Apr;14(4):683-9
16741270
Int J Obes (Lond). 2006 Feb;30(2):288-92
16231018
Expert Opin Investig Drugs. 2005 May;14(5):647-53
15926870
J AOAC Int. 2004 May-Jun;87(3):769-74
15287678
Biochemistry. 2001 Mar 6;40(9):2860-9
11258897
Br J Nutr. 2006 Nov;96(5):795-8
17092365
J Nutr. 2007 Nov;137(11 Suppl):2547S-2551S
17951500
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6874-9
10823914
Br J Nutr. 2005 Apr;93 Suppl 1:S157-61
15877889
Int J Obes Relat Metab Disord. 2004 Aug;28(8):963-71
15197409
J Med Food. 2007 Dec;10(4):720-4
18158848
Trends Endocrinol Metab. 2007 Aug;18(6):240-5
17629492
J Anim Sci. 1997 Sep;75(9):2453-62
9303464
J Nutr. 1993 Nov;123(11):1939-51
8229312
Mol Nutr Food Res. 2005 Jun;49(6):560-70
15926145
Cell Metab. 2006 Mar;3(3):153-65
16517403
Obes Res. 2005 Jun;13(6):1000-7
15976142
Endocr Rev. 2006 Dec;27(7):719-27
17077190
Ann N Y Acad Sci. 2006 Jul;1070:10-26
16888147
J Nutr. 1998 Oct;128(10):1786-93
9772150
Nutrition. 2005 Oct;21(10):1036-43
16157241
J Clin Endocrinol Metab. 2005 Jan;90(1):359-65
15483088
Brain Res. 2005 May 17;1044(1):127-31
15862798
Gastroenterology. 2007 May;132(6):2116-30
17498507
Obesity (Silver Spring). 2006 Sep;14(9):1523-34
17030963
Diabetes. 2006 May;55(5):1484-90
16644709
Clin Ther. 2008 Mar;30(3):513-27
18405789
Br J Nutr. 2004 Sep;92(3):521-6
15469657
Am J Clin Nutr. 1994 Oct;60(4):544-51
8092089
J Biol Chem. 1993 Aug 15;268(23):17247-52
8102366
Diabetes. 1999 Apr;48(4):706-13
10102685
Int J Obes Relat Metab Disord. 2002 Jan;26(1):87-9
11791151
Gastroenterology. 2007 May;132(6):2131-57
17498508
J Endocrinol. 2005 Jun;185(3):457-65
15930172
Endocrinology. 2007 Oct;148(10):4965-73
17584962
J Nutr. 1995 Oct;125(10):2463-70
7562080
Am J Physiol Endocrinol Metab. 2007 Jan;292(1):E238-45
16940471
Am J Clin Nutr. 2001 Feb;73(2 Suppl):415S-420S
11157351
Am J Physiol Endocrinol Metab. 2008 Apr;294(4):E698-708
18285527
Eur J Clin Nutr. 1992 Oct;46 Suppl 2:S33-50
1330528
Nutrition. 1999 Mar;15(3):183-8
10198911