Expression profiling identifies novel gene targets and functions for Pdx1 in the duodenum of mature mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 302, Issue 4, 2012, Pages 407-419

  Chen, Chin ^a   Sibley, Eric ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cre loxP; Intestinal epithelium; Iron metabolism; Lipid metabolism; Microarray

Indexed keywords

ALPHA ACTIN; CERAMIDASE; EPIREGULIN; GASTRIC INHIBITORY POLYPEPTIDE; GLUTATHIONE TRANSFERASE A4; KALLIKREIN; METALLOTHIONEIN I; PERIPHERAL MYELIN PROTEIN 22; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PREALBUMIN; PROTON COUPLED FOLATE TRANSPORTER; SCAVENGER RECEPTOR BI; SOMATOSTATIN; SULFOTRANSFERASE; TRANSCRIPTION FACTOR PDX 1; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; TROPONIN I; VEGETABLE OIL;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR SYSTEM; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CONNECTIVE TISSUE; CONTROLLED STUDY; DOWN REGULATION; DRUG METABOLISM; DUODENUM; ENDOCRINE FUNCTION; ENDOCRINE SYSTEM; FEEDING; FEMALE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE TARGETING; INTESTINE EPITHELIUM; IRON DEFICIENCY; IRON METABOLISM; LAMINA PROPRIA; LIPID ABSORPTION; LIPID METABOLISM; MALE; MEAN CORPUSCULAR HEMOGLOBIN; MEAN CORPUSCULAR VOLUME; MICROARRAY ANALYSIS; MINERAL METABOLISM; MORPHOLOGY; MOUSE; NONHUMAN; NUCLEIC ACID METABOLISM; PRIORITY JOURNAL; RNA ISOLATION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; VITAMIN METABOLISM;

ANIMALS; DUODENUM; ENTEROCYTES; GENE EXPRESSION PROFILING; HOMEODOMAIN PROTEINS; INTESTINAL MUCOSA; IRON; LIPID METABOLISM; MICE; MICE, TRANSGENIC; TRANS-ACTIVATORS;

EID: 84863064170     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00314.2011     Document Type: Article

References (75)

1. Abboud S, Haile DJ. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem 275: 19906-19912, 2000.
2. Alen P, Claessens F, Schoenmakers E, Swinnen JV, Verhoeven G, Rombauts W, Peeters B. Interaction of the putative androgen receptorspecific coactivator ARA70/ELE1alpha with multiple steroid receptors and identification of an internally deleted ELE1beta isoform. Mol Endocrinol 13: 117-128, 1999.
3. Althage MC, Ford EL, Wang S, Tso P, Polonsky KS, Wice BM. Targeted ablation of glucose-dependent insulinotropic polypeptide-producing cells in transgenic mice reduces obesity and insulin resistance induced by a high fat diet. J Biol Chem 283: 18365-18376, 2008.
4. Arnold R, Lankisch PG. Somatostatin and the gastrointestinal tract. Clin Gastroenterol 9: 733-753, 1980.
5. Barley NF, Prathalingam SR, Zhi P, Legon S, Howard A, Walters JR. Factors involved in the duodenal expression of the human calbindin-D9k gene. Biochem J 341: 491-500, 1999.
6. Bates JM, Akerlund J, Mittge E, Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2: 371-382, 2007.
7. Beattie JH, Wood AM, Newman AM, Bremner I, Choo KH, Michalska AE, Duncan JS, Trayhurn P. Obesity and hyperleptinemia in metallothionein (-I and-II) null mice. Proc Natl Acad Sci USA 95: 358-363, 1998.
8. Beaulieu M, Levesque E, Hum DW, Belanger A. Isolation and characterization of a novel cDNA encoding a human UDP-glucuronosyltransferase active on C19 steroids. J Biol Chem 271: 22855-22862, 1996.
9. Bollag RJ, Zhong Q, Phillips P, Min L, Zhong L, Cameron R, Mulloy AL, Rasmussen H, Qin F, Ding KH, Isales CM. Osteoblast-derived cells express functional glucose-dependent insulinotropic peptide receptors. Endocrinology 141: 1228-1235, 2000.
10. Bretherton-Watt D, Gore N, Boam DS. Insulin upstream factor 1 and a novel ubiquitous factor bind to the human islet amyloid polypeptide/ amylin gene promoter. Biochem J 313: 495-502, 1996.
11. Broglio F, Koetsveld Pv P, Benso A, Gottero C, Prodam F, Papotti M, Muccioli G, Gauna C, Hofland L, Deghenghi R, Arvat E, Van Der Lely AJ, Ghigo E. Ghrelin secretion is inhibited by either somatostatin or cortistatin in humans. J Clin Endocrinol Metab 87: 4829-4832, 2002.
12. Brown JC. A gastric inhibitory polypeptide. I. The amino acid composition and the tryptic peptides. Can J Biochem 49: 255-261, 1971.
13. Brown JC, Dryburgh JR. A gastric inhibitory polypeptide. II. The complete amino acid sequence. Can J Biochem 49: 867-872, 1971.
14. Buchan AM, Polak JM, Capella C, Solcia E, Pearse AG. Electronimmunocytochemical evidence for the K cell localization of gastric inhibitory polypeptide (GIP) in man. Histochemistry 56: 37-44, 1978.
15. Carty MD, Lillquist JS, Peshavaria M, Stein R, Soeller WC. Identification of cis-and trans-active factors regulating human islet amyloid polypeptide gene expression in pancreatic beta-cells. J Biol Chem 272: 11986-11993, 1997.
16. Chen C, Fang R, Davis C, Maravelias C, Sibley E. Pdx1 inactivation restricted to the intestinal epithelium in mice alters duodenal gene expression in enterocytes and enteroendocrine cells. Am J Physiol Gastrointest Liver Physiol 297: G1126-G1137, 2009.
17. Chen H, Su T, Attieh ZK, Fox TC, McKie AT, Anderson GJ, Vulpe CD. Systemic regulation of Hephaestin and Ireg1 revealed in studies of genetic and nutritional iron deficiency. Blood 102: 1893-1899, 2003.
18. Cockburn BN, Bermano G, Boodram LL, Teelucksingh S, Tsuchiya T, Mahabir D, Allan AB, Stein R, Docherty K, Bell GI. Insulin promoter factor-1 mutations and diabetes in Trinidad: identification of a novel diabetes-associated mutation (E224K) in an Indo-Trinidadian family. J Clin Endocrinol Metab 89: 971-978, 2004.
19. Collins JF, Franck CA, Kowdley KV, Ghishan FK. Identification of differentially expressed genes in response to dietary iron deprivation in rat duodenum. Am J Physiol Gastrointest Liver Physiol 288: G964-G971, 2005.
20. Dalm VA, Van Hagen PM, de Krijger RR, Kros JM, Van Koetsveld PM, Van Der Lely AJ, Lamberts SW, Hofland LJ. Distribution pattern of somatostatin and cortistatin mRNA in human central and peripheral tissues. Clin Endocrinol (Oxf) 60: 625-629, 2004.
21. Donowitz MWJ, Cusolito S, Sharp GW. Mechanisms of intestinal electrolyte transport and regulation by calcium. In: Pharmacotherapy of Diarrheal Diseases: An Approach Based on Physiologic Principles, edited by Donowitz M SG. New York: Alan R. Liss, 1984.
22. Drucker DJ. The role of gut hormones in glucose homeostasis. J Clin Invest 117: 24-32, 2007.
23. Dupre J, Ross SA, Watson D, Brown JC. Stimulation of insulin secretion by gastric inhibitory polypeptide in man. J Clin Endocrinol Metab 37: 826-828, 1973.
24. Ehses JA, Lee SS, Pederson RA, McIntosh CH. A new pathway for glucose-dependent insulinotropic polypeptide (GIP) receptor signaling: evidence for the involvement of phospholipase A2 in GIP-stimulated insulin secretion. J Biol Chem 276: 23667-23673, 2001.
25. Gannon M, Ables ET, Crawford L, Lowe D, Offield MF, Magnuson MA, Wright CV. Pdx-1 function is specifically required in embryonic beta cells to generate appropriate numbers of endocrine cell types and maintain glucose homeostasis. Dev Biol 314: 406-417, 2008.
26. Gauthier BR, Brun T, Sarret EJ, Ishihara H, Schaad O, Descombes P, Wollheim CB. Oligonucleotide microarray analysis reveals PDX1 as an essential regulator of mitochondrial metabolism in rat islets. J Biol Chem 279: 31121-31130, 2004.
27. Glickman RM, Alpers DH, Drummey GD, Isselbacher KJ. Increased lymph alkaline phosphatase after fat feeding: effects of medium chain triglycerides and inhibition of protein synthesis. Biochim Biophys Acta 201: 226-235, 1970.
28. Gniuli D, Calcagno A, Dalla Libera L, Calvani R, Leccesi L, Caristo ME, Vettor R, Castagneto M, Ghirlanda G, Mingrone G. High-fat feeding stimulates endocrine, glucose-dependent insulinotropic polypeptide (GIP)-expressing cell hyperplasia in the duodenum of Wistar rats. Diabetologia 53: 2233-2240.
29. Goldberg RF, Austen WG Jr, Zhang X, Munene G, Mostafa G, Biswas S, McCormack M, Eberlin KR, Nguyen JT, Tatlidede HS, Warren HS, Narisawa S, Millan JL, Hodin RA. Intestinal alkaline phosphatase is a gut mucosal defense factor maintained by enteral nutrition. Proc Natl Acad Sci USA 105: 3551-3556, 2008.
30. Guz Y, Montminy MR, Stein R, Leonard J, Gamer LW, Wright CV, Teitelman G. Expression of murine STF-1, a putative insulin gene transcription factor, in beta cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny. Development 121: 11-18, 1995.
31. Handley OJ, Naji JJ, Dunnett SB, Rosser AE. Pharmaceutical, cellular and genetic therapies for Huntington's disease. Clin Sci (Lond) 110: 73-88, 2006.
32. Hani EH, Stoffers DA, Chevre JC, Durand E, Stanojevic V, Dina C, Habener JF, Froguel P. Defective mutations in the insulin promoter factor-1 (IPF-1) gene in late-onset type 2 diabetes mellitus. J Clin Invest 104: R41-R48, 1999.
33. Hietanen E. Interspecific variation in the levels of intestinal alkaline phosphatase, adenosine triphosphatase and disaccharidases. Comp Biochem Physiol A 46: 359-369, 1973.
34. Jepeal LI, Fujitani Y, Boylan MO, Wilson CN, Wright CV, Wolfe MM. Cell-specific expression of glucose-dependent-insulinotropic polypeptide is regulated by the transcription factor PDX-1. Endocrinology 146: 383-391, 2005.
35. Jonsson J, Carlsson L, Edlund T, Edlund H. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371: 606-609, 1994.
36. Kirkegaard P, Olsen PS, Nexo E, Holst JJ, Poulsen SS. Effect of vasoactive intestinal polypeptide and somatostatin on secretion of epidermal growth factor and bicarbonate from Brunner's glands. Gut 25: 1225-1229, 1984.
37. Leonard J, Peers B, Johnson T, Ferreri K, Lee S, Montminy MR. Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells. Mol Endocrinol 7: 1275-1283, 1993.
38. Liu J, Liu Y, Hartley D, Klaassen CD, Shehin-Johnson SE, Lucas A, Cohen SD. Metallothionein-I/II knockout mice are sensitive to acetaminophen-induced hepatotoxicity. J Pharmacol Exp Ther 289: 580-586, 1999.
39. Longo FM, Massa SM. Neuroprotective strategies in Alzheimer's disease. NeuroRx 1: 117-127, 2004.
40. Macfarlane WM, Frayling TM, Ellard S, Evans JC, Allen LI, Bulman MP, Ayres S, Shepherd M, Clark P, Millward A, Demaine A, Wilkin T, Docherty K, Hattersley AT. Missense mutations in the insulin promoter factor-1 gene predispose to type 2 diabetes. J Clin Invest 104: R33-R39, 1999.
41. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277: 33275-33283, 2002.
42. Mahmood A, Shao JS, Alpers DH. Rat enterocytes secrete SLPs containing alkaline phosphatase and cubilin in response to corn oil feeding. Am J Physiol Gastrointest Liver Physiol 285: G433-G441, 2003.
43. Mahmood A, Yamagishi F, Eliakim R, DeSchryver-Kecskemeti K, Gramlich TL, Alpers DH. A possible role for rat intestinal surfactant-like particles in transepithelial triacylglycerol transport. J Clin Invest 93: 70-80, 1994.
44. Malo MS, Alam SN, Mostafa G, Zeller SJ, Johnson PV, Mohammad N, Chen KT, Moss AK, Ramasamy S, Faruqui A, Hodin S, Malo PS, Ebrahimi F, Biswas B, Narisawa S, Millan JL, Warren HS, Kaplan JB, Kitts CL, Hohmann EL, Hodin RA. Intestinal alkaline phosphatase preserves the normal homeostasis of gut microbiota. Gut 59: 1476-1484.
45. McIntosh CH. Dipeptidyl peptidase IV inhibitors and diabetes therapy. Front Biosci 13: 1753-1773, 2008.
46. McIntosh CH, Bremsak I, Lynn FC, Gill R, Hinke SA, Gelling R, Nian C, McKnight G, Jaspers S, Pederson RA. Glucose-dependent insulinotropic polypeptide stimulation of lipolysis in differentiated 3T3-L1 cells: wortmannin-sensitive inhibition by insulin. Endocrinology 140: 398-404, 1999.
47. McKie AT, Marciani P, Rolfs A, Brennan K, Wehr K, Barrow D, Miret S, Bomford A, Peters TJ, Farzaneh F, Hediger MA, Hentze MW, Simpson RJ. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell 5: 299-309, 2000.
48. Meijer DK, Scholtens HB, Hardonk MJ. The role of the liver in clearance of glycoproteins from the general circulation, with special reference to intestinal alkaline phosphatase. Pharm Weekbl Sci 4: 57-70, 1982.
49. Miller CP, McGehee RE Jr, Habener JF. IDX-1: a new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostatin gene. EMBO J 13: 1145-1156, 1994.
50. Nakano T, Inoue I, Koyama I, Kanazawa K, Nakamura K, Narisawa S, Tanaka K, Akita M, Masuyama T, Seo M, Hokari S, Katayama S, Alpers DH, Millan JL, Komoda T. Disruption of the murine intestinal alkaline phosphatase gene Akp3 impairs lipid transcytosis and induces visceral fat accumulation and hepatic steatosis. Am J Physiol Gastrointest Liver Physiol 292: G1439-G1449, 2007.
51. Narisawa S, Hoylaerts MF, Doctor KS, Fukuda MN, Alpers DH, Millan JL. A novel phosphatase upregulated in Akp3 knockout mice. Am J Physiol Gastrointest Liver Physiol 293: G1068-G1077, 2007.
52. Narisawa S, Huang L, Iwasaki A, Hasegawa H, Alpers DH, Millan JL. Accelerated fat absorption in intestinal alkaline phosphatase knockout mice. Mol Cell Biol 23: 7525-7530, 2003.
53. Nauck M, Stockmann F, Ebert R, Creutzfeldt W. Reduced incretin effect in type 2 (non-insulin-dependent) diabetes. Diabetologia 29: 46-52, 1986.
54. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, Wright CV. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122: 983-995, 1996.
55. Ohlsson H, Karlsson K, Edlund T. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12: 4251-4259, 1993.
56. Patel YC. Somatostatin and its receptor family. Front Neuroendocrinol 20: 157-198, 1999.
57. Pederson RA, Schubert HE, Brown JC. Gastric inhibitory polypeptide. Its physiologic release and insulinotropic action in the dog. Diabetes 24: 1050-1056, 1975.
58. Penman E, Wass JA, Butler MG, Penny ES, Price J, Wu P, Rees LH. Distribution and characterisation of immunoreactive somatostatin in human gastrointestinal tract. Regul Pept 7: 53-65, 1983.
59. Perley MJ, Kipnis DM. Plasma insulin responses to oral and intravenous glucose: studies in normal and diabetic subjects. J Clin Invest 46: 1954-1962, 1967.
60. Polak JM, Pearse AG, Grimelius L, Bloom SR. Growth-hormone release-inhibiting hormone in gastrointestinal and pancreatic D cells. Lancet 1: 1220-1222, 1975.
61. Serup P, Jensen J, Andersen FG, Jorgensen MC, Blume N, Holst JJ, Madsen OD. Induction of insulin and islet amyloid polypeptide production in pancreatic islet glucagonoma cells by insulin promoter factor 1. Proc Natl Acad Sci USA 93: 9015-9020, 1996.
62. Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, Khan Y, Warley A, McCann FE, Hider RC, Frazer DM, Anderson GJ, Vulpe CD, Simpson RJ, McKie AT. Identification of an intestinal heme transporter. Cell 122: 789-801, 2005.
63. Shi Y, Cheng D. Beyond triglyceride synthesis: the dynamic functional roles of MGAT and DGAT enzymes in energy metabolism. Am J Physiol Endocrinol Metab 297: E10-E18, 2009.
64. Stoffers DA, Stanojevic V, Habener JF. Insulin promoter factor-1 gene mutation linked to early-onset type 2 diabetes mellitus directs expression of a dominant negative isoprotein. J Clin Invest 102: 232-241, 1998.
65. Turgeon D, Carrier JS, Lévesque E, Hum DW, Bélanger A. Relative enzymatic activity, protein stability, and tissue distribution of human steroid-metabolizing UGT2B subfamily members. Endocrinology 142: 778-787, 2001.
66. Usdin TB, Mezey E, Button DC, Brownstein MJ, Bonner TI. Gastric inhibitory polypeptide receptor, a member of the secretin-vasoactive intestinal peptide receptor family, is widely distributed in peripheral organs and the brain. Endocrinology 133: 2861-2870, 1993.
67. Vahl T, D'Alessio D. Enteroinsular signaling: perspectives on the role of the gastrointestinal hormones glucagon-like peptide 1 and glucose-dependent insulinotropic polypeptide in normal and abnormal glucose metabolism. Curr Opin Clin Nutr Metab Care 6: 461-468, 2003.
68. Waeber G, Thompson N, Nicod P, Bonny C. Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol Endocrinol 10: 1327-1334, 1996.
69. Wallace DF, Pedersen P, Dixon JL, Stephenson P, Searle JW, Powell LW, Subramaniam VN. Novel mutation in ferroportin1 is associated with autosomal dominant hemochromatosis. Blood 100: 692-694, 2002.
70. Watada H, Kajimoto Y, Umayahara Y, Matsuoka T, Kaneto H, Fujitani Y, Kamada T, Kawamori R, Yamasaki Y. The human glucokinase gene beta-cell-type promoter: an essential role of insulin promoter factor 1/PDX-1 in its activation in HIT-T15 cells. Diabetes 45: 1478-1488, 1996.
71. Xie QM, Zhang Y, Mahmood S, Alpers DH. Rat intestinal alkaline phosphatase II messenger RNA is present in duodenal crypt and villus cells. Gastroenterology 112: 376-386, 1997.
72. Yip RG, Boylan MO, Kieffer TJ, Wolfe MM. Functional GIP receptors are present on adipocytes. Endocrinology 139: 4004-4007, 1998.
73. Yip RG, Wolfe MM. GIP biology and fat metabolism. Life Sci 66: 91-103, 2000.
74. Yoder SM, Yang Q, Kindel TL, Tso P. Stimulation of incretin secretion by dietary lipid: is it dose dependent? Am J Physiol Gastrointest Liver Physiol 297: G299-G305, 2009.
75. Zhang Y, Shao JS, Xie QM, Alpers DH. Immunolocalization of alkaline phosphatase and surfactant-like particle proteins in rat duodenum during fat absorption. Gastroenterology 110: 478-488, 1996.