Propionate absorbed from the colon acts as gluconeogenic substrate in a strict carnivore, the domestic cat (Felis catus)

Journal of Animal Physiology and Animal Nutrition

Volumn 96, Issue 6, 2012, Pages 1054-1064

  Verbrugghe, A ^a   Hesta, M ^a   Daminet, S ^a   Polis, I ^a   Holst, J J ^b   Buyse, J ^c   Wuyts, B ^d   Janssens, G P J ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LABORATORY OF GENE TECHNOLOGY   (Belgium)

^d GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Acylcarnitine profile; Amino acid metabolism; Cat; Gluconeogenesis; Glucose metabolism; Propionate

Indexed keywords

PROPIONIC ACID; PROPIONIC ACID DERIVATIVE;

ABSORPTION; ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; CAT; COLON; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIET; FEMALE; GLUCONEOGENESIS; MALE; METABOLISM; OBESITY; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL;

ABSORPTION; ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CATS; COLON; CROSS-OVER STUDIES; DIET; FEMALE; GLUCONEOGENESIS; MALE; OBESITY; PROPIONATES;

FELIS CATUS;

EID: 84869097710     PISSN: 09312439     EISSN: 14390396     Source Type: Journal    
DOI: 10.1111/j.1439-0396.2011.01220.x     Document Type: Article

References (58)

1. Anderson, J. W.; Bridges, S. R., 1984: Short-chain fatty-acid fermentation products of plant fiber affect glucose-metabolism of isolated rat hepatocytes. Proceedings of the Society for Experimental Biology and Medicine 177, 372-376.
2. Appleton, D. J.; Rand, J. S.; Priest, J.; Sunvold, G. D., 2001: Determination of reference values for glucose tolerance, insulin tolerance, and insulin sensitivity tests in clinically normal cats. American Journal of Veterinary Research 62, 630-636.
3. Arai, T.; Washizu, T.; Sako, T.; Sasaki, M.; Motoyoshi, S., 1992: D-glucose transport activities in erythrocytes and hepatocytes of dogs, cats and cattle. Comparative Biochemistry & Physiology. Part A, Molecular & Integrative Physiology 102, 285-287.
4. Ballard, F. J., 1965: Glucose utilization in mammalian liver. Comparative Biochemistry & Physiology 14, 437-443.
5. Berggren, A. M.; Nyman, E. M. G. L.; Lundquist, I.; Bjorck, I. M. E., 1996: Influence of orally and rectally administered propionate on cholesterol and glucose metabolism in obese rats. British Journal of Nutrition 76, 287-294.
6. Blair, J. B.; Cook, D. E.; Lardy, H. A., 1973: Interaction of propionate and lactate in perfused rat-liver - effects of glucagon and oleate. The Journal of Biological Chemistry 248, 3608-3614.
7. Boillot, J.; Alamowitch, C.; Berger, A. M.; Luo, J.; Bruzzo, F.; Bornet, F. R.; Slama, G., 1995: Effects of dietary propionate on hepatic glucose production, whole-body glucose utilization, carbohydrate and lipid metabolism in normal rats. British Journal of Nutrition 73, 241-251.
8. Brass, E. P.; Hoppel, C. L., 1980: Relationship between acid-soluble carnitine and coenzyme A pools in vivo. Biochemical Journal 190, 495-504.
9. Bremer, J., 1983: Carnitine - metabolism and functions. Physiological Reviews 63, 1420-1480.
10. Cameron-Smith, D.; Collier, G. R.; Odea, K., 1994: Effect of propionate on in-vivo carbohydrate-metabolism in streptozocin-induced diabetic rats. Metabolism: Clinical and Experimental 43, 728-734.
11. Cani, P. D.; Daubioul, C. A.; Reusens, B.; Remacle, C.; Catillon, G.; Delzenne, N. M., 2005: Involvement of endogenous glucagon-like peptide-1(7-36) amide on glycaemia-lowering effects of oligofructose in streptozotocin-treated rats. Journal of Endocrinology 185, 457-465.
12. Chan, T. M.; Freedland, R. A., 1972: Effect of propionate on metabolism of pyruvate and lactate in perfused rat-liver. Biochemical Journal 127, 539-543.
13. Cuche, G.; Cuber, J. C.; Malbert, C. H., 2000: Ileal short-chain fatty acids inhibit gastric motility by a humoral pathway. American Journal of Physiology. Gastrointestinal & Liver Physiology 279, G925-G930.
14. D'Alessio, D.; Vahl, T.; Prigeon, R., 2004: Effects of glucagon-like peptide-1 on the hepatic glucose metabolism. Hormone & Metabolic Research 36, 837-841.
15. Delzenne, N. M.; Cani, P. D.; Daubioul, C.; Neyrinck, A. M., 2005: Impact of inulin and oligofructose on gastrointestinal peptides. British Journal of Nutrition 93, S157-S161.
16. Delzenne, N. M.; Cani, P. D.; Neyrinck, A. M., 2007: Modulation of glucagon-like peptide 1 and energy metabolism by inulin and oligofructose: experimental data. Journal of Nutrition 137, 2547S-2551S.
17. Drucker, D. J., 2002: Biological actions and therapeutic potential of the glucagon-like peptides. Gastroenterology 122, 531-544.
18. Fahey, G. C.; Flickinger, E. A.; Grieshop, C. M.; Swanson, K. S., 2004: The role of dietary fibre in companion animal nutrition. In: J. W. van der Kamp, N.-G. Asp, J. Miller-Jones, G. Schaafsma (eds), Dietary Fibre - Bio-Active Carbohydrates for Food and Feed. Wageningen Academic Publishers, Wageningen, The Netherlands, pp. 295-328.
19. Freeland, K. R.; Wolever, T. M. S., 2010: Acute effects of intravenous and rectal acetate on glucagon-like peptide-1, petide YY, ghrelin, adiponectin and tumour necrosis factor-α. British Journal of Nutrition 103, 460-466.
20. Hesta, M.; Janssens, G. P. J.; Debraekeleer, J.; De Wilde, R., 2001: The effect of oligofructose and inulin on faecal characteristics and nutrient digestibility in healthy cats. Journal of Animal Physiology and Animal Nutrition 85, 135-141.
21. Hesta, M.; Hoornaert, E.; Verlinden, A.; Janssens, G. P. J., 2005: The effect of oligofructose on urea metabolism and faecal odour components in cats. Journal of Animal Physiology and Animal Nutrition 89, 208-214.
22. Hesta, M.; Debraekeleer, J.; Janssens, G. P. J.; De Wilde, R., 2006: Effects of prebiotics in dog and cat nutrition: a review. In: M. V. Landlow (ed.), Trends in Dietary Carbohydrate Research. Nova Science Publishers, New York, pp. 179-219.
23. Hoenig, M.; Wilkins, C.; Holson, J. C.; Ferguson, D. C., 2003: Effects of obesity on lipid profiles in neutered male and female cats. American Journal of Veterinary Research 64, 299-303.
24. Holst, J. J., 2007: The physiology of glucagon-like peptide 1. Physiological Reviews 87, 1409-1439.
25. Judson, G. J.; Anderson, E.; Luick, J. R.; Leng, R. A., 1968: The contribution of propionate to glucose synthesis in sheep given diets of different grain content. British Journal of Nutrition 22, 69-75.
26. Kley, S.; Hoenig, M.; Glushka, J.; Jin, E. S.; Burgess, S. C.; Waldron, M.; Jordan, E. T.; Prestegard, J. H.; Ferguson, D. C.; Wu, S. X.; Olson, D. E., 2009: The impact of obesity, sex, and diet on hepatic glucose production in cats. American Journal of Physiology. Regulatory Integrative and Comparative Physiology 296, R936-R943.
27. Lovshin, J.; Drucker, D. J., 2000: Synthesis, secretion and biological actions of the glucagon-like peptides. Pediatric Diabetes 1, 49-57.
28. MacDonald, M. L.; Rogers, Q. R.; Morris, J. G., 1984: Nutrition of the domestic cat, a mammalian carnivore. Annual Review of Nutrition 4, 521-562.
29. Martin, G. J. W.; Rand, J. S., 1999: Evaluation of a polyurethane jugular catheter in cats placed using a modified Seldinger technique. Australian Veterinary Journal 77, 250-254.
30. Massimino, S. P.; McBurney, M. I.; Field, C. J.; Thomson, A. B. R.; Keelan, M.; Hayek, M. G.; Sunvold, G. D., 1998: Fermentable dietary fiber increases GLP-1 secretion and improves glucose homeostasis despite increased intestinal glucose transport capacity in healthy dogs. Journal of Nutrition 128, 1786-1793.
31. Morris, J. G., 2002: Idiosyncratic nutrient requirements of cats appear to be diet-induced evolutionary adaptations. Nutrition Research Reviews 15, 153-168.
32. National Research Council, 2006: Energy. In: National Research Council (NRC) (ed.), Nutrient Requirements of Dogs and Cats. The national academies press, Washington, DC, pp. 28-48.
33. Ørskov, C.; Rabenhoj, L.; Wettergren, A.; Kofod, H.; Holst, J. J., 1994: Tissue and plasma-concentrations of amidated and glycine-extended glucagon-like peptide-I in humans. Diabetes 43, 535-539.
34. Petitet, S.; Morand, C.; Besson, C.; Rémésy, C.; Demigné, C., 1998: Effects of propionate on rat hepatocyte metabolism. The Journal of Nutritional Biochemistry 9, 652-658.
35. Prigeon, R. L.; Quddusi, S.; Paty, B.; D'Alessio, D. A., 2003: Suppression of glucose production by GLP-1 independent of islet hormones: a novel extra-pancreatic effect. American Journal of Physiology. Endocrinology & Metabolism 285, E701-E707.
36. Reimer, R. A.; McBurney, M. I., 1996: Dietary fiber modulates intestinal proglucagon messenger ribonucleic acid and postprandial secretion of glucagon-like peptide-1 and insulin in rats. Endocrinology 137, 3948-3956.
37. Reimer, R. A.; Thomson, A. B. R.; Rajotte, R. V.; Basu, T. K.; Ooraikul, B.; McBurney, M. I., 1997: A physiological level of rhubarb fiber increases proglucagon gene expression and modulates intestinal glucose uptake in rats. Journal of Nutrition 127, 1923-1928.
38. Rémésy, C.; Demigné, C.; Morand, C., 2004: Metabolism of short-chain fatty acids in the liver. In: J. H. Cummings, J. L. Rombeau, T. Sakata (eds), Physiological and Clinical Aspects of Short-Chain Fatty Acids. Cambridge University Press, Cambridge, UK, pp. 171-190.
39. Rizzo, C.; Boenzi, S.; Wanders, R. J. A.; Duran, M.; Caruso, U.; Onisi-Vici, C., 2003: Characteristic acylcarnitine profiles in inherited defects of peroxisome biogenesis: a novel tool for screening diagnosis using tandem mass spectrometry. Pediatric Research 53, 1013-1018.
40. Roe, C. R.; Millington, D. S.; Maltby, D. A., 1986: Identification of 3-methylglutarylcarnitine - a new diagnostic metabolite of 3-hydroxy-3-methylglutaryl-coenzyme-A lyase deficiency. Journal of Clinical Investigation 77, 1391-1394.
41. Simmons, H. A.; Ford, E. J. H., 1991: Gluconeogenesis from propionate produced in the colon of the horse. British Veterinary Journal 147, 340-345.
42. Sunvold, G. D.; Hussein, H. S.; Fahey, G. C. Jr; Merchen, N. R.; Reinhart, G. A., 1995: In vitro fermentation of cellulose, beet pulp, citrus pulp, and citrus pectin using fecal inoculum from cats, dogs, horses, humans, and pigs and ruminal fluid from cattle. Journal of Animal Science 73, 3639-3648.
43. Tanaka, A.; Inoue, A.; Takeguchi, A.; Washizu, T.; Bonkobara, M.; Arai, T., 2005: Comparison of expression of glucokinase gene and activities of enzymes related to glucose metabolism in livers between dog and cat. Veterinary Research Communications 29, 477-485.
44. Tappenden, K. A.; McBurney, M. I., 1998: Systemic short-chain fatty acids rapidly alter gastrointestinal structure, function, and expression of early response genes. Digestive Diseases and Science 43, 1526-1536.
45. Tappenden, K. A.; Drozdowski, L. A.; Thomson, A. B. R.; McBurney, M. I., 1998: Short-chain fatty acid-supplemented total parenteral nutrition alters intestinal structure, glucose transporter 2 (GLUT2) mRNA and protein, and proglucagon mRNA abundance in normal rats. American Journal of Clinical Nutrition 68, 118-125.
46. Todesco, T.; Rao, A. V.; Bosello, O.; Jenkins, D. J. A., 1991: Propionate lowers blood-glucose and alters lipid metabolism in healthy-subjects. American Journal of Clinical Nutrition 54, 860-865.
47. Venter, C. S., 1990: Effects of dietary propionate on carbohydrate and lipid-metabolism in healthy-volunteers. American Journal of Gastroenterology 85, 549-553.
48. Verbrugghe, A.; Hesta, M.; Gommeren, K.; Daminet, S.; Wuyts, B.; Buyse, J.; Janssens, G. P. J., 2009: Oligofructose and inulin modulate glucose and amino acid metabolism through propionate production in normal-weight and obese cats. British Journal of Nutrition 102, 694-702.
49. Verbrugghe, A.; Janssens, G. P. J.; Meininger, E.; Daminet, S.; Piron, K.; Vanhaecke, L.; Wuyts, B.; Buyse, J.; Hesta, M., 2010: Intestinal fermentation modulates postprandial acylcarnitine profile and nitrogen metabolism in a true carnivore: the domestic cat (Felis catus). British Journal of Nutrition 104, 972-979.
50. Verbrugghe, A.; Hesta, M.; Daminet, S.; Janssens, G. P. J., 2011: Nutritional modulation of insulin resistance in the true carnivorous cat: a review. Critical reviews in food science and nutrition, accepted.
51. Vreken, P.; van Lint, A. E. M.; Bootsma, A. H.; Overmars, H.; Wanders, R. J. A.; van Gennip, A. H., 1999: Rapid diagnosis of organic acidemias and fatty-acid oxidation defects by quantitative electrospray tandem-MS acyl-carnitine analysis in plasma. In: P. A. Quant, S. Eaton (eds), Current Views of Fatty Acid Oxidation and Ketogenesis - From Organelles to Point Mutations. Kluwer Academic/Plenum Publishers, New York, pp. 327-337.
52. Washizu, T.; Tanaka, A.; Sako, T.; Washizu, M.; Arai, T., 1999: Comparison of the activities of enzymes related to glycolysis and gluconeogenesis in the liver of dogs and cats. Research in Veterinary Science 67, 205-206.
53. Wolever, T. M. S.; Brighenti, F.; Royall, D.; Jenkins, A. L.; Jenkins, D. J. A., 1989: Effect of rectal infusion of short chain fatty-acids in human-subjects. American Journal of Gastroenterology 84, 1027-1033.
54. Wolever, T. M. S.; Spadafora, P.; Eshuis, H., 1991: Interaction between colonic acetate and propionate in humans. American Journal of Clinical Nutrition 53, 681-687.
55. Yost, W. M.; Young, J. W.; Schmidt, S. P.; Mcgilliard, A. D., 1977: Gluconeogenesis in ruminants - propionic-acid production from a high-grain diet fed to cattle. Journal of Nutrition 107, 2036-2043.
56. Zhou, J.; Hegsted, M.; McCutcheon, K. L., 2006: Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity (Silver Spring, Md.) 14, 683-689.
57. Zhou, J.; Martin, R. J.; Tulley, R. T.; Raggio, A. M.; McCutcheon, K. L.; Shen, L.; Danna, S. C.; Tripathy, S.; Hegsted, M.; Keenan, M. J., 2008: Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. American Journal of Physiology. Endocrinology & Metabolism 295, E1160-E1166.
58. Zoran, D. L., 2002: The carnivore connection to nutrition in cats. Journal of the American Veterinary Medical Association 221, 1559-1567.