Regulation of placental amino acid transporter activity by mammalian target of rapamycin

American Journal of Physiology - Cell Physiology

Volumn 296, Issue 1, 2009, Pages

  Roos, S ^a   Kanai, Y ^b   Prasad, P D ^c   Powell, T L ^a,d   Jansson, T ^a,d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b OSAKA UNIVERSITY   (Japan)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

System A; System L; Taurine transporter

Indexed keywords

4F2 HEAVY CHAIN PROTEIN; AMINO ACID TRANSPORTER; ISOPROTEIN; L TYPE AMINO ACID TRANSPORTER 1; L TYPE AMINO ACID TRANSPORTER 2; LACTATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PLACENTA PROTEIN; RAPAMYCIN; SODIUM COUPLED NEUTRAL AMINO ACID TRANSPORTER 1; SODIUM COUPLED NEUTRAL AMINO ACID TRANSPORTER 2; SODIUM COUPLED NEUTRAL AMINO ACID TRANSPORTER 4; TAURINE TRANSPORTER; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TROPHOBLAST;

AMINO ACID TRANSPORT SYSTEM A; AMINO ACID TRANSPORT SYSTEM L; AMINO ACID TRANSPORT SYSTEMS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; FEMALE; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; PREGNANCY; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; TIME FACTORS; TROPHOBLASTS;

MAMMALIA;

EID: 58349106216     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00330.2008     Document Type: Article

References (68)

1. Alberry M, Soothill P. Management of fetal growth restriction. Arch Dis Child Fetal Neonatal Ed 92: F62-F67, 2007.
2. Ananth CV, Wen SW. Trends in fetal growth among singleton gestations in the United States and Canada, 1985 through 1998. Semin Perinatol 26: 260-267, 2002.
3. Asano S, Kameyama M, Oura A, Morisato A, Sakai H, Tabuchi Y, Chairoungdua A, Endou H, Kanai Y. L-type amino acid transporter-1 expressed in human astrocytomas, U343MGa. Biol Pharm Bull 30: 415-422, 2007.
4. Barker DJ. The Wellcome Foundation Lecture, 1994. The fetal origins of adult disease. Proc Biol Sci 262: 37-43, 1995.
5. Bloxam DL, Bax BE, Bax CM. Epidermal growth factor and insulin-like growth factor I differently influence the directional accumulation and transfer of 2-aminoisobutyrate (AIB) by human placental trophoblast in two-sided culture. Biochem Biophys Res Commun 199: 922-929, 1994.
6. Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 115: e290-e296, 2005.
7. Brandsch M, Leibach FH, Mahesh VB, Ganapathy V. Calmodulin-dependent modulation of pH sensitivity of the amino acid transport system L in human placental choriocarcinoma cells. Biochim Biophys Acta 1192: 177-184, 1994.
8. Brodsky D, Christou H. Current concepts in intrauterine growth restriction. J Intensive Care Med 19: 307-319, 2004.
9. Brown NF, Stefanovic-Racic M, Sipula IJ, Perdomo G. The mammalian target of rapamycin regulates lipid metabolism in primary cultures of rat hepatocytes. Metabolism 56: 1500-1507, 2007.
10. Byfield MP, Murray JT, Backer JM. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280: 33076-33082, 2005.
11. Casey BM, Lucas MJ, McIntire DD, Leveno KJ. Pregnancy outcomes in women with gestational diabetes compared with the general obstetric population. Obstet Gynecol 90: 869-873, 1997.
12. Cetin I, Corbetta C, Sereni LP, Marconi AM, Bozzetti P, Pardi G, Battaglia FC. Umbilical amino acid concentrations in normal and growth-retarded fetuses sampled in utero by cordocentesis. Am J Obstet Gynecol 162: 253-261, 1990.
13. Curhan GC, Willett WC, Rimm EB, Spiegelman D, Ascherio AL, Stampfer MJ. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 94: 3246-3250, 1996.
14. Desforges M, Lacey HA, Glazier JD, Greenwood SL, Mynett KJ, Speake PF, Sibley CP. SNAT4 isoform of system A amino acid transporter is expressed in human placenta. Am J Physiol Cell Physiol 290: C305-C312, 2006.
15. Dicke JM, Henderson GI. Placental amino acid uptake in normal and complicated pregnancies. Am J Med Sci 295: 223-227, 1988.
16. Economides DL, Nicolaides KH, Gahl WA, Bernardini I, Evans MI. Plasma amino acids in appropriate- and small-for-gestational-age fetuses. Am J Obstet Gynecol 161: 1219-1227, 1989.
17. Edinger AL. Growth factors regulate cell survival by controlling nutrient transporter expression. Biochem Soc Trans 33: 225-227, 2005.
18. Edinger AL, Linardic CM, Chiang GG, Thompson CB, Abraham RT. Differential effects of rapamycin on mammalian target of rapamycin signaling functions in mammalian cells. Cancer Res 63: 8451-8460, 2003.
19. Edinger AL, Thompson CB. Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol Biol Cell 13: 2276-2288, 2002.
20. Ericsson A, Hamark B, Jansson N, Johansson BR, Powell TL, Jansson T. Hormonal regulation of glucose and system A amino acid transport in first trimester placental villous fragments. Am J Physiol Regul Integr Comp Physiol 288: R656-R662, 2005.
21. Ericsson A, Saljo K, Sjostrand E, Jansson N, Prasad PD, Powell TL, Jansson T. Brief hyperglycaemia in the early pregnant rat increases fetal weight at term by stimulating placental growth and affecting placental nutrient transport. J Physiol 581: 1323-1332, 2007.
22. Findlay GM, Yan L, Procter J, Mieulet V, Lamb RF. A MAP4 kinase related to Ste20 is a nutrient-sensitive regulator of mTOR signalling. Biochem J 403: 13-20, 2007.
23. Furesz TC, Smith CH, Moe AJ. ASC system activity is altered by development of cell polarity in trophoblast from human placenta. Am J Physiol Cell Physiol 265: C212-C217, 1993.
24. Glazier JD, Cetin I, Perugino G, Ronzoni S, Grey AM, Mahendran D, Marconi AM, Pardi G, Sibley CP. Association between the activity of the system A amino acid transporter in the microvillous plasma membrane of the human placenta and severity of fetal compromise in intrauterine growth restriction. Pediatr Res 42: 514-519, 1997.
25. Hennig KM, Colombani J, Neufeld TP. TOR coordinates bulk and targeted endocytosis in the Drosophila melanogaster fat body to regulate cell growth. J Cell Biol 173: 963-974, 2006.
26. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, Hall A, Hall MN. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6: 1122-1128, 2004.
27. Jansson N, Greenwood SL, Johansson BR, Powell TL, Jansson T. Leptin stimulates the activity of the system A amino acid transporter in human placental villous fragments. J Clin Endocrinol Metab 88: 1205-1211, 2003.
28. Jansson N, Pettersson J, Haafiz A, Ericsson A, Palmberg I, Tranberg M, Ganapathy V, Powell TL, Jansson T. Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. J Physiol 576: 935-946, 2006.
29. Jansson T. Amino acid transporters in the human placenta. Pediatr Res 49: 141-147, 2001.
30. Jansson T, Ekstrand Y, Bjorn C, Wennergren M, Powell TL. Alterations in the activity of placental amino acid transporters in pregnancies complicated by diabetes. Diabetes 51: 2214-2219, 2002.
31. Jansson T, Scholtbach V, Powell TL. Placental transport of leucine and lysine is reduced in intrauterine growth restriction. Pediatr Res 44: 532-537, 1998.
32. Jayanthi LD, Ramamoorthy S, Mahesh VB, Leibach FH, Ganapathy V. Substrate-specific regulation of the taurine transporter in human placental choriocarcinoma cells (JAR). Biochim Biophys Acta 1235: 351-360, 1995.
33. Jones HN, Ashworth CJ, Page KR, McArdle HJ. Cortisol stimulates system A amino acid transport and SNAT2 expression in a human placental cell line (BeWo). Am J Physiol Endocrinol Metab 291: E596-E603, 2006.
34. Jones HN, Ashworth CJ, Page KR, McArdle HJ. Expression and adaptive regulation of amino acid transport system A in a placental cell line under amino acid restriction. Reproduction 131: 951-960, 2006.
35. Karl PI. Insulin-like growth factor-1 stimulates amino acid uptake by the cultured human placental trophoblast. J Cell Physiol 165: 83-88, 1995.
36. Karl PI, Alpy KL, Fisher SE. Amino acid transport by the cultured human placental trophoblast: effect of insulin on AIB transport. Am J Physiol Cell Physiol 262: C834-C839, 1992.
37. + permeability: implications for fetal growth. Free Radic Biol Med 36: 271-277, 2004.
38. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF, 3rd. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118: 1567-1582, 1986.
39. Kudo Y, Boyd CA. Heterodimeric amino acid transporters: expression of heavy but not light chains of CD98 correlates with induction of amino acid transport systems in human placental trophoblast. J Physiol 523: 13-18, 2000.
40. Kulanthaivel P, Cool DR, Ramamoorthy S, Mahesh VB, Leibach FH, Ganapathy V. Transport of taurine and its regulation by protein kinase C in the JAR human placental choriocarcinoma cell line. Biochem J 277: 53-58, 1991.
41. Kulanthaivel P, Miyamoto Y, Mahesh VB, Leibach FH, Ganapathy V. Inactivation of taurine transporter by calcium in purified human placental brush border membrane vesicles. Placenta 12: 327-340, 1991.
42. Kuruvilla AG, D'Souza SW, Glazier JD, Mahendran D, Maresh MJ, Sibley CP. Altered activity of the system A amino acid transporter in microvillous membrane vesicles from placentas of macrosomic babies born to diabetic women. J Clin Invest 94: 689-695, 1994.
43. Ling R, Bridges CC, Sugawara M, Fujita T, Leibach FH, Prasad PD, Ganapathy V. Involvement of transporter recruitment as well as gene expression in the substrate-induced adaptive regulation of amino acid transport system A. Biochim Biophys Acta 1512: 15-21, 2001.
44. Liu XM, Reyna SV, Ensenat D, Peyton KJ, Wang H, Schafer AI, Durante W. Platelet-derived growth factor stimulates LAT1 gene expression in vascular smooth muscle: role in cell growth. FASEB J 18: 768-770, 2004.
45. Magnusson-Olsson AL, Lager S, Jacobsson B, Jansson T, Powell TL. Effect of maternal triglycerides and free fatty acids on placental LPL in cultured primary trophoblast cells and in a case of maternal LPL deficiency. Am J Physiol Endocrinol Metab 293: E24-E30, 2007.
46. Mahendran D, Donnai P, Glazier JD, D'Souza SW, Boyd RD, Sibley CP. Amino acid (system A) transporter activity in microvillous membrane vesicles from the placentas of appropriate and small for gestational age babies. Pediatr Res 34: 661-665, 1993.
47. Meller M, Vadachkoria S, Luthy DA, Williams MA. Evaluation of housekeeping genes in placental comparative expression studies. Placenta 26: 601-607, 2005.
48. Nelson DM, Smith SD, Furesz TC, Sadovsky Y, Ganapathy V, Parvin CA, Smith CH. Hypoxia reduces expression and function of system A amino acid transporters in cultured term human trophoblasts. Am J Physiol Cell Physiol 284: C310-C315, 2003.
49. Nobukuni T, Joaquin M, Roccio M, Dann SG, Kim SY, Gulati P, Byfield MP, Backer JM, Natt F, Bos JL, Zwartkruis FJ, Thomas G. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci USA 102: 14238-14243, 2005.
50. Norberg S, Powell TL, Jansson T. Intrauterine growth restriction is associated with a reduced activity of placental taurine transporters. Pediatr Res 44: 233-238, 1998.
51. Okamoto Y, Sakata M, Ogura K, Yamamoto T, Yamaguchi M, Tasaka K, Kurachi H, Tsurudome M, Murata Y. Expression and regulation of 4F2hc and hLAT1 in human trophoblasts. Am J Physiol Cell Physiol 282: C196-C204, 2002.
52. Park SY, Kim JK, Kim IJ, Choi BK, Jung KY, Lee S, Park KJ, Chairoungdua A, Kanai Y, Endou H, Kim DK. Reabsorption of neutral amino acids mediated by amino acid transporter LAT2 and TAT1 in the basolateral membrane of proximal tubule. Arch Pharm Res 28: 421-432, 2005.
53. Peng T, Golub TR, Sabatini DM. The immunosuppressant rapamycin mimics a starvation-like signal distinct from amino acid and glucose deprivation. Mol Cell Biol 22: 5575-5584, 2002.
54. Pettitt DJ, Bennett PH, Saad MF, Charles MA, Nelson RG, Knowler WC. Abnormal glucose tolerance during pregnancy in Pima Indian women. Long-term effects on offspring. Diabetes 40, Suppl 2: 126-130, 1991.
55. Peyrollier K, Hajduch E, Blair AS, Hyde R, Hundal HS. L-Leucine availability regulates phosphatidylinositol 3-kinase, p70 S6 kinase and glycogen synthase kinase-3 activity in L6 muscle cells: evidence for the involvement of the mammalian target of rapamycin (mTOR) pathway in the L-leucine-induced up-regulation of system A amino acid transport. Biochem J 350: 361-368, 2000.
56. Ramamoorthy S, Leibach FH, Mahesh VB, Ganapathy V. Modulation of the activity of amino acid transport system L by phorbol esters and calmodulin antagonists in a human placental choriocarcinoma cell line. Biochim Biophys Acta 1136: 181-188, 1992.
57. Ramamoorthy S, Leibach FH, Mahesh VB, Ganapathy V. Selective impairment of taurine transport by cyclosporin A in a human placental cell line. Pediatr Res 32: 125-127, 1992.
58. Roos S, Jansson NL, Palmberg I, Saljo K, Powell TL, Jansson T. Mammalian target of rapamycin in the human placenta regulates leucine transport and is down-regulated in restricted foetal growth. J Physiol 582: 449-459, 2007.
59. Roos S, Powell TL, Jansson T. Human placental taurine transporter in uncomplicated and IUGR pregnancies: cellular localization, protein expression, and regulation. Am J Physiol Regul Integr Comp Physiol 287: R886-R893, 2004.
60. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22: 159-168, 2006.
61. Shojaiefard M, Christie DL, Lang F. Stimulation of the creatine transporter SLC6A8 by the protein kinase mTOR. Biochem Biophys Res Commun 341: 945-949, 2006.
62. Shojaiefard M, Lang F. Stimulation of the intestinal phosphate transporter SLC34A2 by the protein kinase mTOR. Biochem Biophys Res Commun 345: 1611-1614, 2006.
63. Sipula IJ, Brown NF, Perdomo G. Rapamycin-mediated inhibition of mammalian target of rapamycin in skeletal muscle cells reduces glucose utilization and increases fatty acid oxidation. Metabolism 55: 1637-1644, 2006.
64. Thongsong B, Subramanian RK, Ganapathy V, Prasad PD. Inhibition of amino acid transport system a by interleukin-1beta in trophoblasts. J Soc Gynecol Investig 12: 495-503, 2005.
65. Weisman R, Roitburg I, Nahari T, Kupiec M. Regulation of leucine uptake by tor1+ in Schizosaccharomyces pombe is sensitive to rapamycin. Genetics 169: 539-550, 2005.
66. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell 124: 471-484, 2006.
67. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ. Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol 173: 451-462, 2008.
68. Yusuf K, Smith SD, Sadovsky Y, Nelson DM. Trophoblast differentiation modulates the activity of caspases in primary cultures of term human trophoblasts. Pediatr Res 52: 411-415, 2002.