A glutathione peroxidase, intracellular peptidases and the tor complexes regulate peptide transporter PEPT-1 in C. elegans

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Benner, Jacqueline ^a   Daniel, Hannelore ^a   Spanier, Britta ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE PEROXIDASE; PEPTIDASE; PEPTIDE TRANSPORTER 1; PROTEIN TORC1; PROTEIN TORC2; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG; COTRANSPORTER; DIPEPTIDE; MESSENGER RNA; PEPTIDE HYDROLASE;

ARTICLE; CAENORHABDITIS ELEGANS; CELL STRAIN CACO 2; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME INHIBITION; EPITHELIUM CELL; GENE SILENCING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN MODIFICATION; PROTEIN TRANSPORT; RNA INTERFERENCE; ABSORPTION; ANIMAL; CELL MEMBRANE; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INTRACELLULAR SPACE; METABOLISM; PHYSIOLOGY; PROMOTER REGION; REPRODUCTION; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS; MAMMALIA;

ABSORPTION; ANIMALS; CACO-2 CELLS; CAENORHABDITIS ELEGANS; CELL MEMBRANE; DIPEPTIDES; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GLUTATHIONE PEROXIDASE; HUMANS; INTRACELLULAR SPACE; PEPTIDE HYDROLASES; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; REPRODUCTION; RNA INTERFERENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SYMPORTERS; TOR SERINE-THREONINE KINASES;

EID: 80053228786     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025624     Document Type: Article

References (69)

1. Daniel H, (2004) Molecular and Integrative Physiology of Intestinal Peptide Transport. Annu Rev Physiol 66: 361-384.
2. Fei YJ, Kanai Y, Nussberger S, Ganapathy V, Leibach FH, et al. (1994) Expression cloning of a mammalian proton-coupled oligopeptide transporter. Nature 368: 563-566.
3. Thwaites DT, Anderson CMH, (2007) H+-coupled nutrient, micronutrient and drug transporters in the mammalian small intestine. Exp Physiol 92: 603-619.
4. Rubio-Aliaga I, Daniel H, (2002) Mammalian peptide transporters as targets of drug delivery. Trends Pharmacol Sci 23: 434-440.
5. Rubio-Aliaga I, Daniel H, (2008) Peptide transporters and their roles in physiological processes and drug disposition. Xenobiotica 38: 1022-1042.
6. Daniel H, Spanier B, Kottra G, Weitz D, (2006) From Bateria to Man: Archaic Proton-Dependent Peptide Transports at Work. Physiology 21: 93-102.
7. Thwaites DT, Ford D, Glanville M, Simmons NL, (1999) H+/solute-induced intracellular acidification leads to selective activation of apical Na+/H+ exchange in human intestinal epithelial cells. J Clin Invest 104: 629-635.
8. Thwaites DT, Kennedy DJ, Raldua D, Anderson CMH, Mendoza ME, et al. (2002) H+/dipeptide absorption across the human intestinal epithelium is controlled indirectly via a functional Na+/H+ exchanger. Gastroenterology 122: 1322-1333.
9. Fei YJ, Fujita T, Lapp DF, Ganapathy V, Leibach FH, (1998) Two oligopeptide transporters from Caenorhabditis elegans molecular cloning and functional expression. Biochem J 332: 565-572.
10. Meissner B, Boll M, Daniel H, Baumeister R, (2004) Deletion of the intestinal peptide transporter affects insulin and TOR signaling in Caenorhabditis elegans. J Biol Chem 279: 36739-36745.
11. Nehrke K, (2003) A reduction in intestinal cell pHi due to loss of the Caenorhabditis elegans Na+/H+ exchanger NHX-2 increases lifespan. J Biol Chem 278: 44657-44666.
12. Spanier B, Lasch K, Marsch S, Benner J, Liao W, et al. (2009) How the Intestinal Peptide Transporter PEPT-1 Contributes to an Obesity Phenotype in Caenorhabditis elegans. PLoS One 4: e6279.
13. Gilbert ER, Wong AE, Webb KE jr, (2008) Board-invited review: Peptide absorption and utilization: Implications for animal nutrition and health. J Anim Sci pp. 2135-2155.
14. Boehmer C, Palmada M, Klaus F, Jeyaraj S, Lindner R, et al. (2008) The peptide transporter PEPT2 is targeted by the protein kinase SGK1 and the scaffold protein NHERF2. Cell Physiol Biochem 22: 705-714.
15. Wood WB, (1988) Determination of pattern and fate in early embryos of Caenorhabditis elegans. Dev Biol 5: 57-78.
16. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, et al. (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature Vol 408: 325-330.
17. Kamath RS, Ahringer J, (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
18. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J, (2000) Effectiveness of specific RNA-mediated interference through ingested doublestranded RNA in C. elegans. Genome Biol 2 (I): 0002.1-0002.12.
19. McKay RM, McKay JP, Avery L, Graff JM, (2003) C elegans: a model for exploring the genetics of fat storage. Dev Cell 4: 131-142.
20. Ramakers C, Ruijter JM, Deprez RH, Moorman AF, (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
21. Muller PY, Janovjak H, Miserez AR, Dobbie Z, (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32: 1372-1378.
22. Pauli F, Liu Y, Kim YA, Chen P-J, Kim SK, (2005) Chromosomal clustering and GATA transcriptionalregulation of intestine-expressed genes. Development 133: 287-295.
23. Groneberg DA, Döring F, Eynott PR, Fischer A, Daniel H, (2001) ntestinal peptide transport: ex vivo uptake studies and localization of peptide carrier PEPT1. Am J Physiol Gastrointest. Liver Physiol 281: G697-704.
24. Kennedy DJ, Leibach FH, Ganapathy V, Thwaites DT, (2002) Optimal absorptive transport of the dipeptide glycylsarcosine is dependent on functional Na+/H+ exchange activity. Pflugers Arch 445: 139-146.
25. Brooks KK, Liang B, Watts JL, (2009) The influence of bacterial diet on fat storage in C. elegans. PLoS One 4: e7545.
26. Margis R, Dunand C, Teixeira FK, Margis-Pinheiro M, (2008) Glutathione peroxidase family- an evolutionary overview. FEBS J 275: 3959-3970.
27. Girotti AW, (1998) Lipid hydroperoxide generation, turnover, and effector action in biological systems. J Lipid Res 39 (8): 1529-1542.
28. Otte S, Belden WJ, Heidtman M, Liu J, Jensen ON, et al. (2001) Erv41p and Erv46p: new components of COPII vesicles involved in transport between the ER and Golgi complex. J Cell Biol 152: 503-518.
29. Caldwell SR, Hill KJ, Cooper AA, (2001) Degradation of endoplasmic reticulum (ER) quality control substrates requires transport between the ER and Golgi. J Biol Chem 276: 23296-23303.
30. Veljkovic E, Stasiuk S, Skelly PJ, Shoemaker CB, Verrey F, (2004) Functional Characterization of Caenorhabditis elegans Heteromeric Amino Acid Transporters. J Biol Chem 279: 7655-7662.
31. Schroeder LK, Kremer S, Kramer MJ, Currie E, Kwan E, et al. (2007) Function of the Caenorhabditis elegans ABC transporter PGP-2 in the biogenesis of a lysosome-related fat storage organelle. Mol Biol Cell 18: 995-1008.
32. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, et al. (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421 (6920): 268-72.
33. Rudberg PC, Tholander R, Thunnissen MMGM, Samuelsson B, Haeggström JZ, (2002) Leukotriene A4 hydrolase: Selective abrogation of leukotriene B4 formation by mutation of aspartic acid. PNAS 99: 4215-4220.
34. Orning L, Gierse JK, Fitzpatrick FA, (1994) The bifunctional enzyme leukotriene-A4 hydrolase is an arginine aminopeptidase of high efficiency and specificity. J Biol Chem 269: 11269-11273.
35. Morgan EL, Maskrey BH, Rowley AF, (2005) At what stage in metazoan evolution did leukotriene generation first appear?--key insights from cartilaginous fish. Dev Comp Immunol 29: 53-59.
36. Lenney JF, (1990) Human cytosolic carnosinase: evidence of identity with prolinase, a non-specific dipeptidase. Biol. Chem. Hoppe Seyler 371: 167-171.
37. Ganguli D, Kumar C, Kumar-Bachhawat A, (2007) The Alternative Pathway of Glutathione Degradation Is Mediated by a Novel Protein Complex Involving Three New Genes in Saccharomyces cerevisiae. Genetics 175: 1137-1151.
38. Davies DR, Mamat B, Magnusson OT, Christensen J, Haraldsson MH, et al. (2009) Discovery of leukotriene A4 hydrolase inhibitors using metabolomics biased fragment crystallography. J Med Chem 52: 4694-4715.
39. Teufel M, Saudek V, Ledig JP, Bernhardt A, Boularand S, et al. (2003) Sequence identification and characterization of human carnosinase and a closely related non-specific dipeptidase. J Biol Chem 278: 6521-6531.
40. Daniel H, Adibi SA, (1994) Functional separation of dipeptide transport and hydrolysis in kidney brush border membrane vesicles. FASEB J 8: 753-759.
41. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J, (2005) Rheb binds and regulates the mTOR kinase. Curr Biol 15: 702-713.
42. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, et al. (2008) The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320: 1496-1501.
43. Liu XM, Reyna SV, Ensenat D, Peyton KJ, Wang H, et al. (2004) Platelet-derived growth factor stimulates LAT1 gene expression in vascular smooth muscle: role in cell growth. FASEB J 18: 768-770.
44. Peyrollier K, Hajduch E, Blair AS, Hyde R, Hundal HS, (2000) A role for the actin cytoskeleton in the hormonal and growth-factor-mediated activation of protein kinase B. Biochem J 350: 361-368.
45. Maharoui L, Rodolosse A, Barbat A, Dussaulx E, Zweibaum A, et al. (1994) Presence and differential expression of SGLT1, GLUT1, GLUT2, GLUT3 and GLUT5 hexose-transporter mRNAs in Caco-2 cell clones in relation to cell growth and glucose consumption. Biochem J 298: 629-633.
46. Bao Y, Jemth P, Mannervik B, Williamson G, (1997) Reduction of thymine hydroperoxide by phospholipid hydroperoxide glutathione peroxidase and glutathione transferases. FEBS Lett 410: 210-212.
47. Stenvall J, Fierro-González JC, Swoboda P, Saamarthy K, Cheng Q, et al. (2011) Selenoprotein TRXR-1 and GSR-1 are essential for removal of old cuticle during molting in Caenorhabditis elegans. Proc Natl Acad Sci 108 (3): 1064-9.
48. Taskov K, Chapple C, Kryukov GV, Castellano S, Lobanov AV, et al. (2005) Nematode selenoproteome: the use of the selenocysteine insertion system to decode one codon in an animal genome? Nucleic Acids Res 33 (7): 2227-38.
49. Nomura K, Imai H, Koumura T, Arai M, Nakagawa Y, (1999) Mitochondrial phospholipid hydroperoxide glutathione peroxidase suppresses apoptosis mediated by a mitochondrial death pathway. J Biol Chem 274: 29294-29302.
50. Uchida K, Shiraishi M, Naito Y, Torii Y, Nakamura Y, et al. (1999) Activation of stress signaling pathways by the end product of lipid peroxidation. 4-hydroxy-2-nonenal is a potential inducer of intracellular peroxide production. J Biol Chem 274 (4): 2234-42.
51. Shiraga T, Miyamoto K, Tanaka H, Yamamoto H, Taketani Y, et al. (1999) Cellular and molecular mechanisms of dietary regulation on rat intestinal H+/Peptide transporter PepT1. Gastroenterology 116 (2): 354-62.
52. Haynes CM, Titus E, Cooper A, (2004) Degradation of Misfolded Proteins Prevents ER-Derived Oxidative Stress and Cell Death. Mol Cell 15: 767-776.
53. Bröer S, (2008) Amino Acid Transport Across Mammalian Intestinal and Renal Epithelia. Physiol Rev 88: 249-286.
54. Makky K, Tekiela J, Mayer AN, (2007) Target of rapamycin (TOR) signaling controls epithelial morphogenesis in the vertebrate intestine. Dev Biol 303: 501-13.
55. Rhoads JM, Niu X, Odle J, Graves LM, (2006) Role of mTOR signaling in intestinal cell migration. Am J PhysiolGastrointest Liver Physiol 291: G510-7.
56. Ban H, Shigemitsu K, Yamatsuji T, Haisa M, Nakajo T, et al. (2004) Arginine and Leucine regulate p70 S6 kinase and 4E-BP1 in intestinal epithelial cells. Int J Mol Med 13: 537-43.
57. Rhoads MJ, Wu G, (2009) Glutamine, arginine, and leucine signaling in the intestine. Amino Acids 37: 111-122.
58. Sakiyama T, Musch MW, Ropeleski MJ, Tsubouchi H, Chang EB, (2009) Glutamine increases autophagy under Basal and stressed conditions in intestinal epithelial cells. Gastroenterology 163: 924-32.
59. Long X, Ortiz-Vega S, Lin Y, Avruch J, (2005) Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J Biol Chem 280: 23433-23436.
60. Goberdhan DC, Ogmundsdóttir MH, Kazi S, Reynolds B, Visvalingam SM, et al. (2009) Amino acid sensing and mTOR regulation: inside or out? Biochem Soc Trans 37: 248-252.
61. Das F, Ghosh-Choudhury N, Mahimainathan L, Venkatesan B, Feliers D, et al. (2008) Raptor-rictor axis in TGFbeta-induced protein synthesis. Cell Signal 20: 409-423.
62. Beugnet A, Tee AR, Taylor PM, Proud CG, (2003) Regulation of targets of mTOR (mammalian target of rapamycin) signalling by intracellular amino acid availability. Biochem J 372: 555-566.
63. Dibble CC, Asara JM, Manning BD, (2009) Characterization of Rictor phosphorylation sites reveals direct regulation of mTOR complex 2 by S6K1. Mol Cell Biol 29: 5657-70.
64. Jones KT, Greer ER, Pearce D, Ashrafi K, (2009) Rictor/TORC2 regulates Caenorhabditis elegans fat storage, body size, and development through sgk-1. PLoS Biol 7: e60.
65. Soukas AA, Kane EA, Carr CE, Melo JA, Ruvkun G, (2009) Rictor/TORC2 regulates fat metabolism, feeding, growth, and lifespan in Caenorhabditis elegans. Genes Dev 23: 496-511.
66. Pan KZ, Palter JE, Rogers AN, Olsen A, Chen D, et al. (2007) Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6: 111-119.
67. Long X, Spycher C, Han ZS, Rose AM, Müller F, et al. (2002) TOR deficiency in C. elegans causes developmental arrest and intestinal atrophy by inhibition of mRNA translation. Curr Biol 12: 1448-1461.
68. Jia K, Chen D, Riddle DL, (2004) The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development 131: 3897-3906.
69. Mertl M, Daniel H, Kottra G, (2008) Substrate-induced changes in the density of peptide transporter PEPT1 expressed in Xenopus oocytes. Am J Physiol Cell Physiol 295: C1332-43.