Nerveless and gutsy: Intestinal nutrient sensing from invertebrates to humans

Seminars in Cell and Developmental Biology

Volumn 23, Issue 6, 2012, Pages 614-620

  Miguel Aliaga, Irene ^a  

^a Department of Zoology ^*  (United Kingdom)

Author keywords

Drosophila elegans; Gut; Nutrition; Receptor; Transporter

Indexed keywords

AMINO ACID TRANSPORTER; CARBOHYDRATE; GLUCOSE TRANSPORTER 2; LIPID; PEPTIDE TRANSPORTER 1; PROTEIN; SODIUM GLUCOSE COTRANSPORTER 1; TARGET OF RAPAMYCIN KINASE;

BIOSENSOR; CAENORHABDITIS ELEGANS; CHEMOSENSITIVITY; DROSOPHILA MELANOGASTER; ENTEROENDOCRINE CELL; FOOD INTAKE; GENETIC CONSERVATION; HUMAN; INTESTINAL NUTRIENT SENSING; INTESTINE FUNCTION; INVERTEBRATE; MOLECULAR EVOLUTION; MOLECULAR SENSOR; NONHUMAN; NUTRIENT AVAILABILITY; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TASTE BUD;

CAENORHABDITIS ELEGANS; DROSOPHILA ELEGANS; DROSOPHILA MELANOGASTER; INVERTEBRATA; MAMMALIA;

EID: 84865137460     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.01.002     Document Type: Review

References (114)

1. McIntyre N., Holdsworth C.D., Turner D.S. New interpretation of oral glucose tolerance. Lancet 1964, 2:20-21.
2. Cummings D.E., Overduin J. Gastrointestinal regulation of food intake. J Clin Invest 2007, 117:13-23.
3. Steinert R.E., Beglinger C. Nutrient sensing in the gut: interactions between chemosensory cells, visceral afferents and the secretion of satiation peptides. Physiol Behav 2011, 105:62-70.
4. Berthoud H.R., Kressel M., Raybould H.E., Neuhuber W.L. Vagal sensors in the rat duodenal mucosa: distribution and structure as revealed by in vivo DiI-tracing. Anat Embryol (Berl) 1995, 191:203-212.
5. Johnson L.R. Physiology of the gastrointestinal tract 2006, Elsevier, San Diego.
6. Behrens M., Meyerhof W. Gustatory and extragustatory functions of mammalian taste receptors. Physiol Behav 2011, 105:4-13.
7. Broer S. Apical transporters for neutral amino acids: physiology and pathophysiology. Physiology (Bethesda) 2008, 23:95-103.
8. Broer S. Amino acid transport across mammalian intestinal and renal epithelia. Physiol Rev 2008, 88:249-286.
9. Palacin M., Nunes V., Font-Llitjos M., Jimenez-Vidal M., Fort J., Gasol E., et al. The genetics of heteromeric amino acid transporters. Physiology (Bethesda) 2005, 20:112-124.
10. Young R.L. Sensing via intestinal sweet taste pathways. Front Neurosci 2011, 5:23.
11. Helliwell P.A., Richardson M., Affleck J., Kellett G.L. Stimulation of fructose transport across the intestinal brush-border membrane by PMA is mediated by GLUT2 and dynamically regulated by protein kinase C. Biochem J 2000, 350(Pt 1):149-154.
12. Kellett G.L., Brot-Laroche E., Mace O.J., Leturque A. Sugar absorption in the intestine: the role of GLUT2. Annu Rev Nutr 2008, 28:35-54.
13. Lindquist B., Meeuwisse G.W. Chronic diarrhoea caused by monosaccharide malabsorption. Acta Paediatr 1962, 51:674-685.
14. Wright E.M., Turk E., Martin M.G. Molecular basis for glucose-galactose malabsorption. Cell Biochem Biophys 2002, 36:115-121.
15. +-d-glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes 2012, 61:187-196.
16. Baggio L.L., Drucker D.J. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007, 132:2131-2157.
17. McLaughlin S.K., McKinnon P.J., Margolskee R.F. Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature 1992, 357:563-569.
18. Wong G.T., Gannon K.S., Margolskee R.F. Transduction of bitter and sweet taste by gustducin. Nature 1996, 381:796-800.
19. Hofer D., Asan E., Drenckhahn D. Chemosensory perception in the gut. News Physiol Sci 1999, 14:18-23.
20. Hofer D., Puschel B., Drenckhahn D. Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc Natl Acad Sci USA 1996, 93:6631-6634.
21. Jang H.J., Kokrashvili Z., Theodorakis M.J., Carlson O.D., Kim B.J., Zhou J., et al. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA 2007, 104:15069-15074.
22. +-glucose cotransporter 1. Proc Natl Acad Sci USA 2007, 104:15075-15080.
23. Wu S.V., Rozengurt N., Yang M., Young S.H., Sinnett-Smith J., Rozengurt E. Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc Natl Acad Sci USA 2002, 99:2392-2397.
24. Kokrashvili Z., Mosinger B., Margolskee R.F. Taste signaling elements expressed in gut enteroendocrine cells regulate nutrient-responsive secretion of gut hormones. Am J Clin Nutr 2009, 90:822S-825S.
25. Dyer J., Daly K., Salmon K.S., Arora D.K., Kokrashvili Z., Margolskee R.F., et al. Intestinal glucose sensing and regulation of intestinal glucose absorption. Biochem Soc Trans 2007, 35:1191-1194.
26. Au A., Gupta A., Schembri P., Cheeseman C.I. Rapid insertion of GLUT2 into the rat jejunal brush-border membrane promoted by glucagon-like peptide 2. Biochem J 2002, 367:247-254.
27. Mace O.J., Affleck J., Patel N., Kellett G.L. Sweet taste receptors in rat small intestine stimulate glucose absorption through apical GLUT2. J Physiol 2007, 582:379-392.
28. Le Gall M., Tobin V., Stolarczyk E., Dalet V., Leturque A., Brot-Laroche E. Sugar sensing by enterocytes combines polarity, membrane bound detectors and sugar metabolism. J Cell Physiol 2007, 213:834-843.
29. Ford H.E., Peters V., Martin N.M., Sleeth M.L., Ghatei M.A., Frost G.S., et al. Effects of oral ingestion of sucralose on gut hormone response and appetite in healthy normal-weight subjects. Eur J Clin Nutr 2011, 65:508-513.
30. Fujita Y., Wideman R.D., Speck M., Asadi A., King D.S., Webber T.D., et al. Incretin release from gut is acutely enhanced by sugar but not by sweeteners in vivo. Am J Physiol Endocrinol Metab 2009, 296:E473-E479.
31. Ma J., Bellon M., Wishart J.M., Young R., Blackshaw L.A., Jones K.L., et al. Effect of the artificial sweetener, sucralose, on gastric emptying and incretin hormone release in healthy subjects. Am J Physiol Gastrointest Liver Physiol 2009, 296:G735-G739.
32. Cani P.D., Holst J.J., Drucker D.J., Delzenne N.M., Thorens B., Burcelin R., et al. GLUT2 and the incretin receptors are involved in glucose-induced incretin secretion. Mol Cell Endocrinol 2007, 276:18-23.
33. Parker H.E., Habib A.M., Rogers G.J., Gribble F.M., Reimann F. Nutrient-dependent secretion of glucose-dependent insulinotropic polypeptide from primary murine K cells. Diabetologia 2009, 52:289-298.
34. Reimann F., Habib A.M., Tolhurst G., Parker H.E., Rogers G.J., Gribble F.M. Glucose sensing in L cells: a primary cell study. Cell Metab 2008, 8:532-539.
35. Moriya R., Shirakura T., Ito J., Mashiko S., Seo T. Activation of sodium-glucose cotransporter 1 ameliorates hyperglycemia by mediating incretin secretion in mice. Am J Physiol Endocrinol Metab 2009, 297:E1358-E1365.
36. Rogers G.J., Tolhurst G., Ramzan A., Habib A.M., Parker H.E., Gribble F.M., et al. Electrical activity-triggered glucagon-like peptide-1 secretion from primary murine L-cells. J Physiol 2011, 589:1081-1093.
37. Bennett K., James C., Hussain K. Pancreatic beta-cell KATP channels: hypoglycaemia and hyperglycaemia. Rev Endocr Metab Disord 2010, 11:157-163.
38. Morgan E.L., Mace O.J., Affleck J., Kellett G.L. Apical GLUT2 and Cav1.3: regulation of rat intestinal glucose and calcium absorption. J Physiol 2007, 580:593-604.
39. Morgan E.L., Mace O.J., Helliwell P.A., Affleck J., Kellett G.L. A role for Ca(v)1.3 in rat intestinal calcium absorption. Biochem Biophys Res Commun 2003, 312:487-493.
40. Mace O.J., Morgan E.L., Affleck J.A., Lister N., Kellett G.L. Calcium absorption by Cav1.3 induces terminal web myosin II phosphorylation and apical GLUT2 insertion in rat intestine. J Physiol 2007, 580:605-616.
41. Cassany A., Guillemain G., Klein C., Dalet V., Brot-Laroche E., Leturque A. A karyopherin alpha2 nuclear transport pathway is regulated by glucose in hepatic and pancreatic cells. Traffic 2004, 5:10-19.
42. Guillemain G., Munoz-Alonso M.J., Cassany A., Loizeau M., Faussat A.M., Burnol A.F., et al. Karyopherin alpha2: a control step of glucose-sensitive gene expression in hepatic cells. Biochem J 2002, 364:201-209.
43. Guillemain G., Loizeau M., Pincon-Raymond M., Girard J., Leturque A. The large intracytoplasmic loop of the glucose transporter GLUT2 is involved in glucose signaling in hepatic cells. J Cell Sci 2000, 113(Pt 5):841-847.
44. Fafournoux P., Bruhat A., Jousse C. Amino acid regulation of gene expression. Biochem J 2000, 351:1-12.
45. Jefferson L.S., Kimball S.R. Amino acids as regulators of gene expression at the level of mRNA translation. J Nutr 2003, 133:2046S-2051S.
46. Kilberg M.S., Pan Y.X., Chen H., Leung-Pineda V. Nutritional control of gene expression: how mammalian cells respond to amino acid limitation. Annu Rev Nutr 2005, 25:59-85.
47. Kim J., Guan K.L. Amino acid signaling in TOR activation. Annu Rev Biochem 2011, 80:1001-1032.
48. van Sluijters D.A., Dubbelhuis P.F., Blommaart E.F., Meijer A.J. Amino-acid-dependent signal transduction. Biochem J 2000, 351(Pt 3):545-550.
49. Dockray G.J. Luminal sensing in the gut: an overview. J Physiol Pharmacol 2003, 54(Suppl. 4):9-17.
50. Tolhurst G., Reimann F., Gribble F.M. Nutritional regulation of glucagon-like peptide-1 secretion. J Physiol 2009, 587:27-32.
51. Choi S., Lee M., Shiu A.L., Yo S.J., Hallden G., Aponte G.W. GPR93 activation by protein hydrolysate induces CCK transcription and secretion in STC-1 cells. Am J Physiol Gastrointest Liver Physiol 2007, 292:G1366-G1375.
52. Reimann F., Williams L., da Silva Xavier G., Rutter G.A., Gribble F.M. Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells. Diabetologia 2004, 47:1592-1601.
53. Matsumura K., Miki T., Jhomori T., Gonoi T., Seino S. Possible role of PEPT1 in gastrointestinal hormone secretion. Biochem Biophys Res Commun 2005, 336:1028-1032.
54. Didion T., Regenberg B., Jorgensen M.U., Kielland-Brandt M.C., Andersen H.A. The permease homologue Ssy1p controls the expression of amino acid and peptide transporter genes in Saccharomyces cerevisiae. Mol Microbiol 1998, 27:643-650.
55. Hundal H.S., Taylor P.M. Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am J Physiol Endocrinol Metab 2009, 296:E603-E613.
56. Donaton M.C., Holsbeeks I., Lagatie O., Van Zeebroeck G., Crauwels M., Winderickx J., et al. The Gap1 general amino acid permease acts as an amino acid sensor for activation of protein kinase A targets in the yeast Saccharomyces cerevisiae. Mol Microbiol 2003, 50:911-929.
57. Erickson R.H., Gum J.R., Lindstrom M.M., McKean D., Kim Y.S. Regional expression and dietary regulation of rat small intestinal peptide and amino acid transporter mRNAs. Biochem Biophys Res Commun 1995, 216:249-257.
58. Mace O.J., Lister N., Morgan E., Shepherd E., Affleck J., Helliwell P., et al. An energy supply network of nutrient absorption coordinated by calcium and T1R taste receptors in rat small intestine. J Physiol 2009, 587:195-210.
59. Terada T., Inui K. Gene expression and regulation of drug transporters in the intestine and kidney. Biochem Pharmacol 2007, 73:440-449.
60. Hu Y., Smith D.E., Ma K., Jappar D., Thomas W., Hillgren K.M. Targeted disruption of peptide transporter Pept1 gene in mice significantly reduces dipeptide absorption in intestine. Mol Pharm 2008, 5:1122-1130.
61. Nassl A.M., Rubio-Aliaga I., Sailer M., Daniel H. The intestinal peptide transporter PEPT1 is involved in food intake regulation in mice fed a high-protein diet. PLoS One 2011, 6:e26407.
62. Little T.J., Feinle-Bisset C. Effects of dietary fat on appetite and energy intake in health and obesity-oral and gastrointestinal sensory contributions. Physiol Behav 2011, 104:613-620.
63. Beglinger S., Drewe J., Schirra J., Goke B., D'Amato M., Beglinger C. Role of fat hydrolysis in regulating glucagon-like Peptide-1 secretion. J Clin Endocrinol Metab 2010, 95:879-886.
64. McLaughlin J., Grazia Luca M., Jones M.N., D'Amato M., Dockray G.J., Thompson D.G. Fatty acid chain length determines cholecystokinin secretion and effect on human gastric motility. Gastroenterology 1999, 116:46-53.
65. Hirasawa A., Tsumaya K., Awaji T., Katsuma S., Adachi T., Yamada M., et al. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 2005, 11:90-94.
66. Edfalk S., Steneberg P., Edlund H. Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 2008, 57:2280-2287.
67. Liou A.P., Lu X., Sei Y., Zhao X., Pechhold S., Carrero R.J., et al. The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin. Gastroenterology 2011, 140:903-912.
68. Dew S.E., Ong D.E. Specificity of the retinol transporter of the rat small intestine brush border. Biochemistry 1994, 33:12340-12345.
69. Chen M., Yang Y., Braunstein E., Georgeson K.E., Harmon C.M. Gut expression and regulation of FAT/CD36: possible role in fatty acid transport in rat enterocytes. Am J Physiol Endocrinol Metab 2001, 281:E916-E923.
70. Laugerette F., Passilly-Degrace P., Patris B., Niot I., Febbraio M., Montmayeur J.P., et al. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J Clin Invest 2005, 115:3177-3184.
71. Drover V.A., Ajmal M., Nassir F., Davidson N.O., Nauli A.M., Sahoo D., et al. CD36 deficiency impairs intestinal lipid secretion and clearance of chylomicrons from the blood. J Clin Invest 2005, 115:1290-1297.
72. Glatzle J., Darcel N., Rechs A.J., Kalogeris T.J., Tso P., Raybould H.E. Apolipoprotein A-IV stimulates duodenal vagal afferent activity to inhibit gastric motility via a CCK1 pathway. Am J Physiol Regul Integr Comp Physiol 2004, 287:R354-R359.
73. Glatzle J., Kalogeris T.J., Zittel T.T., Guerrini S., Tso P., Raybould H.E. Chylomicron components mediate intestinal lipid-induced inhibition of gastric motor function. Am J Physiol Gastrointest Liver Physiol 2002, 282:G86-G91.
74. Fu J., Gaetani S., Oveisi F., Lo Verme J., Serrano A., Rodriguez De Fonseca F., et al. Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 2003, 425:90-93.
75. Schwartz G.J., Fu J., Astarita G., Li X., Gaetani S., Campolongo P., et al. The lipid messenger OEA links dietary fat intake to satiety. Cell Metab 2008, 8:281-288.
76. Ashrafi K., Chang F.Y., Watts J.L., Fraser A.G., Kamath R.S., Ahringer J., et al. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 2003, 421:268-272.
77. Chen L.Q., Hou B.H., Lalonde S., Takanaga H., Hartung M.L., Qu X.Q., et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 2010, 468:527-532.
78. Carvalho G.B., Kapahi P., Anderson D.J., Bender S. Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Curr Biol 2006, 16:692-696.
79. Cognigni P., Bailey A.P., Miguel-Aliaga I. Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab 2011, 13:92-104.
80. de Bono M., Sokolowski M. Foraging in flies and worms. Invertebrate neurobiology 2007, 437-466. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. G. North, R.J. Greenspan (Eds.).
81. Ribeiro C., Dickson B.J. Sex peptide receptor and neuronal TOR/S6K signaling modulate nutrient balancing in Drosophila. Curr Biol 2010, 20:1000-1005.
82. Apidianakis Y., Rahme L.G. Drosophila melanogaster as a model for human intestinal infection and pathology. Dis Model Mech 2011, 4:21-30.
83. Montell C. A taste of the Drosophila gustatory receptors. Cur Opin Neurobiol 2009, 19:345-353.
84. Sato K., Tanaka K., Touhara K. Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci USA 2011, 108:11680-11685.
85. Bifano T.D., Alegria T.G., Terra W.R. Transporters involved in glucose and water absorption in the Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) anterior midgut. Comp Biochem Physiol B Biochem Mol Biol 2010, 157:1-9.
86. Caccia S., Casartelli M., Grimaldi A., Losa E., de Eguileor M., Pennacchio F., et al. Unexpected similarity of intestinal sugar absorption by SGLT1 and apical GLUT2 in an insect (Aphidius ervi, Hymenoptera) and mammals. Am J Physiol Regul Integr Comp Physiol 2007, 292:R2284-R2291.
87. Caccia S., Leonardi M.G., Casartelli M., Grimaldi A., de Eguileor M., Pennacchio F., et al. Nutrient absorption by Aphidius ervi larvae. J Insect Physiol 2005, 51:1183-1192.
88. Price D.R., Tibbles K., Shigenobu S., Smertenko A., Russell C.W., Douglas A.E., et al. Sugar transporters of the major facilitator superfamily in aphids; from gene prediction to functional characterization. Insect Mol Biol 2010, 19(Suppl 2):97-112.
89. Price D.R., Wilkinson H.S., Gatehouse J.A. Functional expression and characterisation of a gut facilitative glucose transporter, NlHT1, from the phloem-feeding insect Nilaparvata lugens (rice brown planthopper). Insect Biochem Mol Biol 2007, 37:1138-1148.
90. Escher S.A., Rasmuson-Lestander A. The Drosophila glucose transporter gene: cDNA sequence, phylogenetic comparisons, analysis of functional sites and secondary structures. Hereditas 1999, 130:95-103.
91. Park J.H., Kwon J.Y. Heterogeneous expression of Drosophila gustatory receptors in enteroendocrine cells. PLoS One 2011, 6:e29022.
92. Fei Y.J., Fujita T., Lapp D.F., Ganapathy V., Leibach F.H. Two oligopeptide transporters from Caenorhabditis elegans: molecular cloning and functional expression. Biochem J 1998, 332(Pt 2):565-572.
93. Fei Y.J., Romero M.F., Krause M., Liu J.C., Huang W., Ganapathy V., et al. A novel H(+)-coupled oligopeptide transporter (OPT3) from Caenorhabditis elegans with a predominant function as a H(+) channel and an exclusive expression in neurons. J Biol Chem 2000, 275:9563-9571.
94. Meissner B., Boll M., Daniel H., Baumeister R. Deletion of the intestinal peptide transporter affects insulin and TOR signaling in Caenorhabditis elegans. J Biol Chem 2004, 279:36739-36745.
95. Nehrke K. A reduction in intestinal cell pHi due to loss of the Caenorhabditis elegans Na+/H+ exchanger NHX-2 increases life span. J Biol Chem 2003, 278:44657-44666.
96. Martin F.P., Spanier B., Collino S., Montoliu I., Kolmeder C., Giesbertz P., et al. Metabotyping of Caenorhabditis elegans and their culture media revealed unique metabolic phenotypes associated to amino acid deficiency and insulin-like signaling. J Proteome Res 2011, 10:990-1003.
97. Spanier B., Lasch K., Marsch S., Benner J., Liao W., Hu H., et al. How the intestinal peptide transporter PEPT-1 contributes to an obesity phenotype in Caenorhabditits elegans. PLoS One 2009, 4:e6279.
98. Roman G., Meller V., Wu K.H., Davis R.L. The opt1 gene of Drosophila melanogaster encodes a proton-dependent dipeptide transporter. Am J Physiol 1998, 275:C857-C869.
99. Goberdhan D.C., Meredith D., Boyd C.A., Wilson C. PAT-related amino acid transporters regulate growth via a novel mechanism that does not require bulk transport of amino acids. Development 2005, 132:2365-2375.
100. Hansen I.A., Boudko D.Y., Shiao S.H., Voronov D.A., Meleshkevitch E.A., Drake L.L., et al. AaCAT1 of the yellow fever mosquito, Aedes aegypti: a novel histidine-specific amino acid transporter from the SLC7 family. J Biol Chem 2011, 286:10803-10813.
101. Reynolds B., Roversi P., Laynes R., Kazi S., Boyd C.A., Goberdhan D.C. Drosophila expresses a CD98 transporter with an evolutionarily conserved structure and amino acid-transport properties. Biochem J 2009, 420:363-372.
102. Boudko D.Y., Kohn A.B., Meleshkevitch E.A., Dasher M.K., Seron T.J., Stevens B.R., et al. Ancestry and progeny of nutrient amino acid transporters. Proc Natl Acad Sci USA 2005, 102:1360-1365.
103. Castagna M., Shayakul C., Trotti D., Sacchi V.F., Harvey W.R., Hediger M.A. Cloning and characterization of a potassium-coupled amino acid transporter. Proc Natl Acad Sci USA 1998, 95:5395-5400.
104. --independent. J Biol Chem 2000, 275:24518-24526.
105. Miller M.M., Popova L.B., Meleshkevitch E.A., Tran P.V., Boudko D.Y. The invertebrate B(0) system transporter, D. melanogaster NAT1, has unique d-amino acid affinity and mediates gut and brain functions. Insect Biochem Mol Biol 2008, 38:923-931.
106. Thimgan M.S., Berg J.S., Stuart A.E. Comparative sequence analysis and tissue localization of members of the SLC6 family of transporters in adult Drosophila melanogaster. J Exp Biol 2006, 209:3383-3404.
107. Colombani J., Raisin S., Pantalacci S., Radimerski T., Montagne J., Leopold P. A nutrient sensor mechanism controls Drosophila growth. Cell 2003, 114:739-749.
108. Martin J.F., Hersperger E., Simcox A., Shearn A. Minidiscs encodes a putative amino acid transporter subunit required non-autonomously for imaginal cell proliferation. Mech Dev 2000, 92:155-167.
109. Britton J.S., Edgar B.A. Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 1998, 125:2149-2158.
110. Attardo G.M., Hansen I.A., Shiao S.H., Raikhel A.S. Identification of two cationic amino acid transporters required for nutritional signaling during mosquito reproduction. J Exp Biol 2006, 209:3071-3078.
111. Hennig K.M., Colombani J., Neufeld T.P. TOR coordinates bulk and targeted endocytosis in the Drosophila melanogaster fat body to regulate cell growth. J Cell Biol 2006, 173:963-974.
112. Meleshkevitch E.A., Assis-Nascimento P., Popova L.B., Miller M.M., Kohn A.B., Phung E.N., et al. Molecular characterization of the first aromatic nutrient transporter from the sodium neurotransmitter symporter family. J Exp Biol 2006, 209:3183-3198.
113. +-tryptophan symporter, AgNAT6. J Exp Biol 2009, 212:1559-1567.
114. +-aromatic amino acid symporters in the model alimentary canal of mosquito larvae. J Exp Biol 2008, 211:1594-1602.