Increased expression of system large amino acid transporter (LAT)-1 mRNA is associated with invasive potential and unfavorable prognosis of human clear cell renal cell carcinoma

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Betsunoh, Hironori ^a   Fukuda, Takehiko ^a   Anzai, Naohiko ^a   Nishihara, Daisaku ^a   Mizuno, Tomoya ^a   Yuki, Hideo ^a   Masuda, Akinori ^a   Yamaguchi, Yoshiyuki ^a   Abe, Hideyuki ^a   Yashi, Masahiro ^a   Fukabori, Yoshitatsu ^a   Yoshida, Ken Ichiro ^a   Kamai, Takao ^a  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 F2 CELL SURFACE ANTIGEN; AMINO ACID TRANSPORTER; LARGE AMINO ACID TRANSPORTER 1; LARGE AMINO ACID TRANSPORTER 2; LARGE AMINO ACID TRANSPORTER 3; LARGE AMINO ACID TRANSPORTER 4; MEMBRANE ANTIGEN; MESSENGER RNA; S6 KINASE; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; FEMALE; FOLLOW UP; GENE EXPRESSION; HUMAN; HUMAN TISSUE; KIDNEY CARCINOMA; MAJOR CLINICAL STUDY; MALE; METASTASIS POTENTIAL; OVERALL SURVIVAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR DIFFERENTIATION; TUMOR INVASION; WESTERN BLOTTING;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, RENAL CELL; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION; HUMANS; KIDNEY NEOPLASMS; LARGE NEUTRAL AMINO ACID-TRANSPORTER 1; MALE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM STAGING; PHOSPHORYLATION; PROGNOSIS; RIBOSOMAL PROTEIN S6; RNA, MESSENGER;

EID: 84886555397     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-509     Document Type: Article

References (51)

1. Motzer RJ, Bander NH, Nanus DM. Renal-cell carcinoma. N Engl J Med 1996, 335:865-875. 10.1056/NEJM199609193351207, 8778606.
2. Athar U, Gentile TC. Treatment options for metastatic renal cell carcinoma: a review. Can J Urol 2008, 15:523-532.
3. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011, 331:1559-1564. 10.1126/science.1203543, 21436443.
4. De Berardinis RJ, Julian JL, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuelscell growth and proliferation. Cell Metab 2008, 7:11-20. 10.1016/j.cmet.2007.10.002, 18177721.
5. Barger JF, Plas DR. Balancing biosynthesis and bioenergetics: metabolic programs in oncogenesis. Endocr Relat Cancer 2010, 17:R287-R304. 10.1677/ERC-10-0106, 20699334.
6. Christensen HN. Role of amino acid transport and countertransport in nurtrition and metabolism. Physiol Rev 1990, 70:43-77.
7. McGivan JD, Pastor-Anglada M. Regulatory and molecular aspects of mammalian amino acid transport. Biochem J 1994, 299:321-334. 1138275, 8172590.
8. Ganapathy V, Thangaraju M, Prasad PD. Nutrient transporters in caner: relevance to Warburg hypothesis and beyond. Pharmacol THer 2009, 121:29-40. 10.1016/j.pharmthera.2008.09.005, 18992769.
9. Kanai Y, Segawa H, Miyamoto K, Uchino H, Takeda E, Endou H. Expression cloning and characterization of a transporter for large neutral amino acids activated by the heavy chain of 4 F2 antigen (CD98). J Biol Chem 1998, 273:23629-23632. 10.1074/jbc.273.37.23629, 9726963.
10. Yanagida O, Kanai Y, Chairoungdua A, Kim DK, Segawa H, Nii T, Cha SH, Matsuo H, Fukushima J, Fukasawa Y, Tani Y, Taketani Y, Uchino H, Kim JY, Inatomi J, Okayasu I, Miyamoto K, Takeda E, Goya T, Endou H. Human L-type amino acid transporter 1 (LAT1): characterization of function and expression in tumor cell lines. Biochim Biophys Acta 2001, 1514:291-302. 10.1016/S0005-2736(01)00384-4, 11557028.
11. Kobayashi H, Ishii Y, Takayama T. Expression of L-type amino acid transporter 1 (LAT1) in esophageal carcinoma. J Surg Oncol 2005, 90:233-238. 10.1002/jso.20257, 15906366.
12. Nawashiro H, Otani N, Shinomiya N, Fukui S, Ooigawa H, Shima K, Matsuo H, Kanai Y, Endou H. L-type amino acid transporter 1 as a potential molecular target in human astrocytic tumors. Int J Cancer 2006, 119:484-492. 10.1002/ijc.21866, 16496379.
13. Kaira K, Oriuchi N, Imai H, Shimizu K, Yanagitani N, Sunaga N, Hisada T, Tanaka S, Ishizuka T, Kanai Y, Endou H, Nakajima T, Mori M. Prognostic significance of L-type amino acid transporter 1 expression in resectable stage I-III nonsmall cell lung cancer. Br J Cancer 2008, 98:742-748. 10.1038/sj.bjc.6604235, 2259171, 18253116.
14. Ichinoe M, Mikami T, Yoshida T, Igawa I, Tsuruta T, Nakada N, Anzai N, Suzuki Y, Endou H, Okayasu I. High expression of L-type amino acid transporter 1 (LAT1) in gastric carcinomas: comparison with non-cancerous lesions. Pathol Int 2011, 61:281-289. 10.1111/j.1440-1827.2011.02650.x, 21501294.
15. Nakanishi K, Ogata S, Matsui H, Kanai Y, Endou H, Hiroi S, Tominaga S, Aida S, Kasamatsu H, Kawai T. Expression of LAT1 predicts risk of progression of transitional cell carcinoma of the upper urinary tract. Virchows Arch 2007, 451:681-690. 10.1007/s00428-007-0457-9, 17622555.
16. Sakata T, Ferdous G, Tsuruta T, Satoh T, Baba S, Muto T, Ueno A, Kanai Y, Endou H, Okayasu I. L-type amino acid transporter 1 as a novel biomarker for high-grade malignancy in prostate cancer. Pathol Int 2009, 59:7-18. 10.1111/j.1440-1827.2008.02319.x, 19121087.
17. Oda K, Hosoda N, Endo H, Saito K, Tsujihara K, Yamamura M, Sakata T, Anzai N, Wempe MF, Kanai Y, Endou H. L-type amino acid transporter 1 inhibitors inhibit tumor cell growth. Cancer Sci 2010, 101:173-179. 10.1111/j.1349-7006.2009.01386.x, 19900191.
18. Wagner CA, Lang F, Broer S. Function and structure of heterodimeric acid transporters. Am J Physio Cell Physiol 2001, 281:c1077-c1093.
19. Babu E, Kanai Y, Chairoungdua A, Kim DK, Iribe Y, Tangtrongsup S, Jutabha P, Li Y, Ahmed N, Sakamoto S, Anzai N, Nagamori S, Endou H. Identification of a novel system L amino acid transporter structurally distinct from heterodimeric amino acid transporters. J Biol Chem 2003, 278:43838-43845. 10.1074/jbc.M305221200, 12930836.
20. Bodoy S, Martín L, Zorzano A, Palacín M, Estévez R, Bertran J. Identification of LAT4, a novel amino acid transporter with system L activity. J Biol Chem 2005, 280:12002-12022. 10.1074/jbc.M408638200, 15659399.
21. Kurayama R, Ito N, Nishibori Y, Fukuhara D, Akimoto Y, Higashihara E, Ishigaki Y, Sai Y, Miyamoto K, Endou H, Kanai Y, Yan K. Role of amino acid transporter LAT2 in the activation of mTORC1 pathway and the pathogenesis of crescentic glomerulonephritis. Lab Invest 2011, 91:992-1006. 10.1038/labinvest.2011.43, 21403644.
22. Sekine Y, Nishibori Y, Akimoto Y, Kudo A, Ito N, Fukuhara D, Kurayama R, Higashihara E, Babu E, Kanai Y, Asanuma K, Nagata M, Majumdar A, Tryggvason K, Yan K. Amino acid transporter LAT3 is required for podocyte development and function. J Am Soc Nephrol 2009, 20:1586-1596. 10.1681/ASN.2008070809, 2709689, 19443642.
23. Suwa H, Ohshio G, Imamura T, Watanabe G, Arii S, Imamura M, Narumiya S, Hiai H, Fukumoto M. Overexpression of the rhoC gene correlates with progression of ductal adenocarcinoma of the pancreas. Br J Cancer 1998, 77:147-152. 10.1038/bjc.1998.23, 2151257, 9459160.
24. Kamai T, Yanai Y, Arai K, Abe H, Yamanishi T, Kurimoto M, Yoshida K-I. Increased interferon alpha receptor 2 mRNA levels is associated with renal cell carcinoma metastasis. BMC Cancer 2007, 7:1471-2407. 7-159.
25. Fuhrman SA, Lasky LC, Lmas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 1982, 6:655-663. 10.1097/00000478-198210000-00007, 7180965.
26. Sobin LH, Gospodarowicz MK, Wittekind CH. International union against cancer. UICC. TNM classification of malignant tumors 2009, 255-257. New York: Wiley-Liss, 7.
27. Kamai T, Tsujii T, Arai K, Takagi K, Asami H, Ito Y, Oshima H, Yoshida K-I. Significant association of Rho/ROCK pathway with invasion and metastasis of bladder cancer. Clin Cancer Res 2003, 9:2632-2641.
28. Furuya N, Kamai T, Shirataki H, Yanai Y, Fukuda T, Mizuno T, Kambara T, Nakanishi K, Abe H, Yoshida K-I. Serum interferon alpha receptor 2 mRNA may predict efficacy of interferon alpha with/without low-dose sorafenib for metastatic clear cell renal cell carcinoma. Cancer Immunol Immunother 2011, 60:793-808. 10.1007/s00262-011-0989-3, 3098978, 21350947.
29. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033. 10.1126/science.1160809, 2849637, 19460998.
30. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674. 10.1016/j.cell.2011.02.013, 21376230.
31. Oxender DL, Christensen HN. Evidence for two types of mediation of neutral amino acid transport in Ehrlich cells. Nature 1963, 197:765-767. 10.1038/197765a0, 13940861.
32. Novick AC. Open surgery of the kidney. Campbell-Walsh Urology 2007, 1686-1758. Philadelphia: Saunders Elsevier, Wein AJ, Kavoussi LR, Novick AC, Partin AW, Peters CA, 9.
33. Fuchs BC, Bode BP. Amino acid transporters ASCT2 and LAT1 in cancer: partners in crime?. Semin Cancer Biol 2005, 15:254-266. 10.1016/j.semcancer.2005.04.005, 15916903.
34. Yamauchi K, Sakurai H, Kimura T, Wiriyasermkul P, Nagamori S, Kanai Y, Kohno N. System L amino acid transporter inhibitor enhances anti-tumor activity of cisplatin in a head and neck squamous cell carcinoma cell line. Cancer Lett 2009, 276:95-101. 10.1016/j.canlet.2008.10.035, 19058911.
35. Imai H, Kaira K, Oriuchi N, Shimizu K, Tominaga H, Yanagitani N, Sunaga N, Ishizuka T, Nagamori S, Promchan K, Nakajima T, Yamamoto N, Mori M, Kanai Y. Inhibition of L-type amino acid transporter 1 has antitumor activity in non-small cell lung cancer. Anticancer Res 2010, 30:4819-4828.
36. Wang Q, Bailey CG, Ng C, Tiffen J, Thoeng A, Minhas V, Lehman ML, Hendy SC, Buchanan G, Nelson CC, Rasko JE, Holst J. Androgen receptor and nutrient signaling pathways coordinate the demand for increased amino acid transport during prostate cancer progression. Cancer Res 2011, 71:7525-7536. 10.1158/0008-5472.CAN-11-1821, 22007000.
37. Abe H, Kamai T. Recent advances in the treatment of metastatic renal cell carcinoma. Int J Urol 2013, 10.1111 In publication.
38. Hudes G, Carducci M, Tomczak P, Dutcher J, Figlin R, Kapoor A, Staroslawska E, Sosman J, McDermott D, Bodrogi I, Kovacevic Z, Lesovoy V, Schmidt-Wolf IG, Barbarash O, Gokmen E, O'Toole T, Lustgarten S, Moore L, Motzer RJ. Global ARCC trial : temsirolimus, interferon Alfa, or both for advanced renal-cell carcinoma. N Engl J Med 2007, 356:2271-2281. 10.1056/NEJMoa066838, 17538086.
39. Motzer RJ, Escudier B, Oudard S, Hutson TE, Porta C, Bracarda S, Grünwald V, Thompson JA, Figlin RA, Hollaender N, Urbanowitz G, Berg WJ, Kay A, Lebwohl D, Ravaud A. RECORD-1 study group: efficacy of everolimus in advanced renal cell carcinoma: a double-blind, randomised, placebo-controlled phase III trial. Lancet 2008, 372:449-456. 10.1016/S0140-6736(08)61039-9, 18653228.
40. Hayashi K, Jutabha P, Endou H, Anzai N. c-Myc is crucial for the expression of LAT1 in MIA paca-2 human pancreatic cancer cells. Oncol Rep 2012, 28:862-866.
41. Kim JW, Zeller KI, Wang Y, Jegga AG, Aronow BJ, O'Donnell KA, Dang CV. Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Mol Cell Biol 2004, 24:5923-5936. 10.1128/MCB.24.13.5923-5936.2004, 480875, 15199147.
42. Osthus RC, Shim H, Kim S, Li Q, Reddy R, Mukherjee M, Xu Y, Wonsey D, LA LA, Dang CV. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 2000, 275:21797-21800. 10.1074/jbc.C000023200, 10823814.
43. Dang CV, Le A, Gao P. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin Cancer Res 2009, 15:6479-6483. 10.1158/1078-0432.CCR-09-0889, 2783410, 19861459.
44. Dang CV. Rethinking the Warburg effect with Myc micromanaging glutamine metabolism. Cancer Res 2010, 70:859-862. 10.1158/0008-5472.CAN-09-3556, 2818441, 20086171.
45. Tang SW, Chang WH, Su YC, Chen YC, Lai YH, Wu PT, Hsu CI, Lin WC, Lai MK, Lin JY. MYC pathway is activated in clear cell renal cell carcinoma and essential for proliferation of clear cell renal cell carcinoma. Cancer Lett 2009, 273:35-43. 10.1016/j.canlet.2008.07.038, 18809243.
46. Liu Y, Yin B, Zhang C, Zhou L, Fan J. Has-let-7a functions as a tumor suppressor in renal cell carcinoma cell lines by targeting c-myc. Biochem Biophys Res Commun 2012, 417:371-375. 10.1016/j.bbrc.2011.11.119, 22155254.
47. Luo X, Yin P, Reierstad S, Ishikawa H, Lin Z, Pavone ME, Zhao H, Marsh EE, Bulun SE. Progesterone and Mifepristone regulate L-type amino acid transporter 2 and 4 F2 heavy chain expression in uterine leiomyoma cells. J Clin Endocrinol Metab 2009, 94:4533-4539. 10.1210/jc.2009-1286, 2775649, 19808856.
48. Kaira K, Ohde Y, Endo M, Nakagawa K, Okumura T, Takahashi T, Murakami H, Tsuya A, Nakamura Y, Naito T, Kondo H, Nakajima T, Yamamoto N. Expression of 4F2hc (CD98) in pulmonary neuroendocrine tumors. Oncol Rep 2011, 26:931-937.
49. Takeuchi H, Kubota T, Kitai R, Nakagawa T, Hashimoto N. CD98 immunoreactivity in multinucleated giant cells of glioblastomas: an immunohistochemical double labeling study. Neuropathology 2008, 28:127-131. 10.1111/j.1440-1789.2007.00859.x, 18021193.
50. Kaira K, Oriuchi N, Shimizu K, Ishikita T, Higuchi T, Imai H, Yanagitani N, Sunaga N, Hisada T, Ishizuka T, Kanai Y, Endou H, Nakajima T, Endo K, Mori M. Correlation of angiogenesis with 18 F-FMT and 18 F-FDG uptake in non-small cell lung cancer. Cancer Sci 2009, 100:753-758. 10.1111/j.1349-7006.2008.01077.x, 19141127.
51. Kaira K, Oriuchi N, Imai H, Shimizu K, Yanagitani N, Sunaga N, Hisada T, Kawashima O, Kamide Y, Ishizuka T, Kanai Y, Nakajima T, Mori M. CD98 expression is associated with poor prognosis in resected non-small cell lung cancer with lymph node metastasis. Ann Surg Oncol 2009, 16:3437-3481.