Role of amino acid transporter LAT2 in the activation of mTORC1 pathway and the pathogenesis of crescentic glomerulonephritis

Laboratory Investigation

Volumn 91, Issue 7, 2011, Pages 992-1006

  Kurayama, Ryota ^a   Ito, Noriko ^a   Nishibori, Yukino ^a   Fukuhara, Daisuke ^a   Akimoto, Yoshihiro ^a   Higashihara, Eiji ^a   Ishigaki, Yasuhito ^b   Sai, Yoshimichi ^c   Miyamoto, Ken Ichi ^c   Endou, Hitoshi ^a   Kanai, Yoshikatstu ^d   Yan, Kunimasa ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

^c KANAZAWA UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

branched chain amino acid; crescentic glomerulonephritis; everolimus; LAT; mTORC1

Indexed keywords

2 AMINO 2 NORBORNATE CARBOXYLIC ACID; AMINO ACID TRANSPORTER; CARBOXYLIC ACID; EVEROLIMUS; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN LAT1; PROTEIN LAT2; PROTEIN LAT3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL MEMBRANE; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; NONHUMAN; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAPIDLY PROGRESSIVE GLOMERULONEPHRITIS; RAT; SIGNAL TRANSDUCTION;

AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; ANTIGENS, CD98 LIGHT CHAINS; BASE SEQUENCE; BLOTTING, WESTERN; DNA PRIMERS; FEMALE; GLOMERULONEPHRITIS; IMMUNOHISTOCHEMISTRY; RATS; RATS, INBRED WKY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 79959755211     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.43     Document Type: Article

References (57)

1. Wiggins RC HL, Legault DJ. Glomerular inflammation and crescent formation. In: Neilson EG, Couser WG (eds). Immunologic Renal Diseases. Lippincott-Raven: Philadelphia, 1997, pp 669-682.
2. Magil AB. Histogenesis of glomerular crescents. Immunohistochemical demonstration of cytokeratin in crescent cells. Am J Pathol 1985;120: 222-229. (Pubitemid 16255954)
3. Morita T, Suzuki Y, Churg J. Structure and development of the glomerular crescent. Am J Pathol 1973;72:349-368.
4. Min KW, Gyorkey F, Gyorkey P, et al. The morphogenesis of glomerular crescents in rapidly progressive glomerulonephritis. Kidney Int 1974;5:47-56.
5. Ophascharoensuk V, Pippin JW, Gordon KL, et al. Role of intrinsic renal cells versus infiltrating cells in glomerular crescent formation. Kidney Int 1998;54:416-425. (Pubitemid 28357404)
6. Guettier C, Nochy D, Jacquot C, et al. Immunohistochemical demonstration of parietal epithelial cells and macrophages in human proliferative extra-capillary lesions. Virchows Archiv 1986;409: 739-748. (Pubitemid 16043909)
7. Le Hir M, Keller C, Eschmann V, et al. Podocyte bridges between the tuft and Bowman's capsule: an early event in experimental crescentic glomerulonephritis. J Am Soc Nephrol 2001;12: 2060-2071. (Pubitemid 32880342)
8. Moeller MJ, Soofi A, Hartmann I, et al. Podocytes populate cellular crescents in a murine model of inflammatory glomerulonephritis. J Am Soc Nephrol 2004;15:61-67. (Pubitemid 38020698)
9. Smeets B, Uhlig S, Fuss A, et al. Tracing the origin of glomerular extracapillary lesionfrom parietal epitherial cells. J Am Soc Nephrol 2009;20:2604-2615.
10. Abboud HE. Growth factors in glomerulonephritis. Kidney Int 1993;43:252-267.
11. Kitching AR, Turner AL, Wilson GR, et al. IL-12p40 and IL-18 in crescentic glomerulonephritis: IL-12p40 is the key Th1-defining cytokine chain, whereas IL-18 promotes local inflammation and leukocyte recruitment. J Am Soc Nephrol 2005;16:2023-2033. (Pubitemid 41716433)
12. Lloyd CM, Minto AW, Dorf ME, et al. RANTES and monocyte chemoattractant protein-1 (MCP-1) play an important role in the inflammatory phase of crescentic nephritis, but only MCP-1 is involved in crescent formation and interstitial fibrosis. J Exp Med 1997;185: 1371-1380. (Pubitemid 27172917)
13. Song CY, Kim BC, Hong HK, et al. TGF-beta type II receptor deficiency prevents renal injury via decrease in ERK activity in crescentic glomerulonephritis. Kidney Int 2007;71:882-888. (Pubitemid 46663790)
14. Ono K, Han J. The p38 signal transduction pathway: activation and function. Cell Signal 2000;12:1-13. (Pubitemid 30017963)
15. Deng T, Karin M. c-Fos transcriptional activity stimulated by H-Rasactivated protein kinase distinct from JNK and ERK. Nature 1994;371:171-175. (Pubitemid 24284018)
16. Lee JC, Laydon JT, McDonnell PC, et al. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 1994;372:739-746.
17. Bokemeyer D, Guglielmi KE, McGinty A, et al. Activation of extracellular signal-regulated kinase in proliferative glomerulonephritis in rats. J Clin Invest 1997;100:582-588. (Pubitemid 27340505)
18. Polzer K, Soleiman A, Baum W, et al. Selective p38MAPK isoform expression and activation in antineutrophil cytoplasmatic antibodyassociated crescentic glomerulonephritis: role of p38MAPKalpha. Ann Rheum Dis 2008;67:602-608. (Pubitemid 351571921)
19. Dann SG, Thomas G. The amino acid sensitive TOR pathway from yeast to mammals. FEBS Lett 2006;580:2821-2829. (Pubitemid 43729161)
20. Yang Q, Guan KL. Expanding mTOR signaling. Cell Res 2007;17: 666-681. (Pubitemid 47255937)
21. Wang X, Campbell LE, Miller CM, et al. Amino acid availability regulates p70 S6 kinase and multiple translation factors. Biochem J 1998;334:261-267. (Pubitemid 28420997)
22. Proud CG. mTOR-mediated regulation of translation factors by amino acids. Biochem Biophys Res Commun 2004;313:429-436. (Pubitemid 37543604)
23. Kim E. Mechanisms of amino acid sensing in mTOR signaling pathway. Nutr Res Pract 2009;3:64-71.
24. Fox HL, Pham PT, Kimball SR, et al. Amino acid effects on translational repressor 4E-BP1 are mediated primarily by L-leucine in isolated adipocytes. Am J Physiol 1998;275:C1232-C1238.
25. Christensen HN. Role of amino acid transport and countertransport in nutrition and metabolism. Physiol Rev 1990;70:43-77. (Pubitemid 20037281)
26. Palacin M, Estevez R, Bertran J, et al. Molecular biology of mammalian plasma membrane amino acid transporters. Physiol Rev 1998;78: 969-1054. (Pubitemid 28491947)
27. Kanai Y, Segawa H, Miyamoto K, et al. Expression cloning and characterization of a transporter for large neutral amino acids activated by the heavy chain of 4F2 antigen (CD98). J Biol Chem 1998;273:23629-23632. (Pubitemid 28435687)
28. Yanagida O, Kanai Y, Chairoungdua A, et al. Human L-type amino acid transporter 1 (LAT1): characterization of function and expression in tumor cell lines. Biochim Biophys Acta 2001;1514:291-302. (Pubitemid 32831016)
29. Nakanishi K, Matsuo H, Kanai Y, et al. LAT1 expression in normal lung and in atypical adenomatous hyperplasia and adenocarcinoma of the lung. Virchows Arch 2006;448:142-150. (Pubitemid 43237879)
30. Matsuo H, Tsukada S, Nakata T, et al. Expression of a system L neutral amino acid transporter at the blood-brain barrier. Neuroreport 2000;11:3507-3511.
31. Kageyama T, Nakamura M, Matsuo A, et al. The 4F2hc/LAT1 complex transports L-DOPA across the blood-brain barrier. Brain Res 2000;879:115-121.
32. Ritchie JW, Taylor PM. Role of the system L permease LAT1 in amino acid and iodothyronine transport in placenta. Biochem J 2001;356:719-725. (Pubitemid 32588443)
33. Park SY, Kim JK, Kim IJ, et al. Reabsorption of neutral amino acids mediated by amino acid transporter LAT2 and TAT1 in the basolateral membrane of proximal tubule. Arch Pharm Res 2005;28:421-432.
34. Dave MH, Schulz N, Zecevic M, et al. Expression of heteromeric amino acid transporters along the murine intestine. J Physiol 2004;558:597-610. (Pubitemid 39117604)
35. Pineda M, Fernandez E, Torrents D, et al. Identification of a membrane protein, LAT-2, that co-expresses with 4F2 heavy chain, an L-type amino acid transport activity with broad specificity for small and large zwitterionic amino acids. J Biol Chem 1999;274:19738-19744.
36. Segawa H, Fukasawa Y, Miyamoto K, et al. Identification and functional characterization of a Na+-independent neutral amino acid transporter with broad substrate selectivity. J Biol Chem 1999;274:19745-19751.
37. Rossier G, Meier C, Bauch C, et al. LAT2, a new basolateral 4F2hc/CD98- associated amino acid transporter of kidney and intestine. J Biol Chem 1999;274:34948-34954. (Pubitemid 129509543)
38. Sekine Y, Nishibori Y, Akimoto Y, et al. Amino acid transporter LAT3 is required for podocyte development and function. J Am Soc Nephrol 2009;20:1586-1596.
39. Bodoy S, Martin L, Zorzano A, et al. Identification of LAT4, a novel amino acid transporter with system Lactivity. J Biol Chem 2005;280:12002-12011. (Pubitemid 40418518)
40. Kohda T, Okada S, Hayashi A, et al. High nephritogenicity of monoclonal antibodies belonging to IgG2a and IgG2b subclasses in rat anti-GBM nephritis. Kidney Int 2004;66:177-186. (Pubitemid 38870093)
41. Treberg JR, Clow KA, Greene KA, et al. Systemic activation of glutamate dehydrogenase: implications for the hyperinsulinism/hyperammonemia syndrome. Am J Physiol Endocrinol Metab 2010;298:E1219-E1225.
42. Morimoto E, Kanai Y, Kim do K, et al. Establishment and characterization of mammalian cell lines stably expressing human L-type amino acid transporters. J Pharmacol Sci 2008;108:505-516.
43. Seeliger H, Guba M, Kleespies A, et al. Role of mTOR in solid tumor systems: a therapeutical target against primary tumor growth, metastases, and anigiogenesis. Cancer Metastasis Rev 2007;26: 611-621. (Pubitemid 350115107)
44. Fox HL, Kimball SR, Jefferson LS, et al. Amino acids stimulate phosphorylation of p70S6k and organization of rat adipocytes into multicellular clusters. Am J Physiol 1998;274:C206-C213.
45. Foster KG, Fingar DC. mTOR: conducting the cellular signaling symphony. J Biol Chem 2010;285:14071-14077.
46. Fingar DC, Richardson CJ, Tee AR, et al. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/ eukaryotic translation initiation factor 4E. Mol Cell Biol 2004;24: 200-216. (Pubitemid 38010048)
47. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004;18:1926-1945. (Pubitemid 39071573)
48. Lieberthal W, Levine JS. The role of the mammalian target of rapamycin (mTOR) in renal disease. J Am Soc Nephrol 2009;20:2493-2502.
49. Lieberthal W, Fuhro R, Andry CC, et al. Rapamycin impairs recovery from acute renal failure: role of cell-cycle arrest and apoptosis of tubular cells. Am J Physiol Renal Physiol 2001;281:F693-F706.
50. Mariappan MM, Feliers D, Mummidi S, et al. High glucose, high insulin, and their combination rapidly induce laminin-beta1 synthesis by regulation of mRNA translation in renal epithelial cells. Diabetes 2007;56:476-485.
51. Chen JK, Chen J, Neilson EG, et al. Role of mammalian target of rapamycin signaling in compensatory renal hypertrophy. J Am Soc Nephrol 2005;16:1384-1391. (Pubitemid 41716522)
52. Hochegger K, Jansky GL, Soleiman A, et al. Differential effects of rapamycin in anti-GBM glomerulonephritis. J Am Soc Nephrol 2008;19:1520-1529.
53. Cornish GH, Sinclair LV, Cantrell DA. Differential regulation of T-cell growth by IL-2 and IL-15. Blood 2006;108:600-608. (Pubitemid 44061360)
54. Edinger AL, Thompson CB. Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol Biol Cell 2002;13:2276-2288. (Pubitemid 34831333)
55. Nii T, Segawa H, Taketani Y, et al. Molecular events involved in upregulating human Na+-independent neutral amino acid transporter LAT1 during T-cell activation. Biochem J 2001;358:693-704. (Pubitemid 32896957)
56. Ishizuka Y, Kakiya N, Nawa H, et al. Leucine induces phosphorylation and activation of p70S6K in cortical neurons via the system Lamino acid transporter. J Neurochem 2008;106:934-942.
57. Edinger AL. Controlling cell growth and survival through regulated nutrient transporter expression. Biochem J 2007;406:1-12. (Pubitemid 47264729)