EphrinA1 inhibits malignant mesothelioma tumor growth via let-7 microRNA-mediated repression of the RAS oncogene

Cancer Gene Therapy

Volumn 18, Issue 11, 2011, Pages 806-816

  Khodayari, N ^a   Mohammed, K A ^a,b   Goldberg, E P ^c   Nasreen, N ^a,c  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

EphrinA1; let 7 microRNA; malignant mesothelioma; RAS

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; EPHRIN A1; EPHRIN RECEPTOR A2; MICRORNA; RNA PRECURSOR;

ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; LET 7 GENE; MALIGNANT MESOTHELIOMA; ONCOGENE H RAS; ONCOGENE K RAS; ONCOGENE N RAS; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN INDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING;

CELL GROWTH PROCESSES; EPHRIN-A1; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, RAS; HUMANS; MESOTHELIOMA; MICRORNAS; PLEURAL NEOPLASMS; RECEPTOR, EPHA2; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION;

EID: 80054720177     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2011.50     Document Type: Article

References (46)

1. Mutsaers SE. The mesothelial cell. Int J Biochem Cell Biol 2004; 36: 9-16. (Pubitemid 37338468)
2. Leppla SH, Arora N, Varughese M. Anthrax toxin fusion proteins for intracellular delivery of macromolecules. J Appl Microbiol 1999; 87: 284.
3. Murer B. Pleural malignant mesothelioma. Adv Clin Pathol 2000; 4: 177-179.
4. Baas P, Schouwink H, Zoetmulder FA. Malignant pleural mesothelioma. Ann Oncol 1998; 9: 139-149. (Pubitemid 28123615)
5. Moore S, Darlison L, Tod AM. Living with mesothelioma. A literature review. Eur J Cancer Care 2010; 19: 458-468.
6. Drescher U, Kremoser C, Handwerker C, Loschinger J, Noda M, Bonhoeffer F. In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 1995; 82: 359-370.
7. Macrae M, Neve RM, Rodriguez-Viciana P, Haqq C, Yeh J, Chen C et al. A conditional feedback loop regulates Ras activity through EphA2. Cancer cell 2005; 8: 111-118. (Pubitemid 41132740)
8. McBride JL, Ruiz JC. Ephrin-A1 is expressed at sites of vascular development in the mouse. Mech Dev 1998; 77: 201-204. (Pubitemid 28545172)
9. Wykosky J, Debinski W. The EphA2 receptor and ephrinA1 ligand in solid tumors: function and therapeutic targeting. Mol Cancer Res 2008; 6: 1795-1806.
10. Noblitt LW, Bangari DS, Shukla S, Knapp DW, Mohammed S, Kinch MS et al. Decreased tumorigenic potential of EphA2-overexpressing breast cancer cells following treatment with adenoviral vectors that express EphrinA1. Cancer Gene Ther 2004; 11: 757-766. (Pubitemid 39488474)
11. Duxbury MS, Ito H, Zinner MJ, Ashley SW, Whang EE. Ligation of EphA2 by Ephrin A1-Fc inhibits pancreatic adenocarcinoma cellular invasiveness. Biochem Biophys Res Commun 2004; 320: 1096-1102. (Pubitemid 38916656)
12. Lai YM, Mohammed KA, Nasreen N, Baumuratov A, Bellew BF, Antony VB. Induction of cell cycle arrest and apoptosis by BCG infection in cultured human bronchial airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2007; 293: L393-L401. (Pubitemid 47205020)
13. Pratt RL, Kinch MS. Ligand binding up-regulates EphA2 messenger RNA through the mitogen-activated protein/extracellular signal-regulated kinase pathway. Mol Cancer Res 2003; 1: 1070-1076. (Pubitemid 38044982)
14. Self AJ, Caron E, Paterson HF, Hall A. Analysis of R-Ras signalling pathways. J Cell Sci 2001; 114: 1357-1366. (Pubitemid 32409471)
15. Patel MR, Jacobson BA, De A, Frizelle SP, Janne P, Thumma SC et al. Ras pathway activation in malignant mesothelioma. J Thorac Oncol 2007; 2: 789-795. (Pubitemid 47361018)
16. Eskandarpour M, Huang F, Reeves KA, Clark E, Hansson J. Oncogenic NRAS has multiple effects on the malignant phenotype of human melanoma cells cultured in vitro. Int J Cancer 2009; 124: 16-26.
17. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 2006; 6: 259-269.
18. Ricarte Filho JC, Kimura ET. MicroRNAs: novel class of gene regulators involved in endocrine function and cancer. Arq Bras Endocrinol Metabol 2006; 50: 1102-1107.
19. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin1-4. Cell 1993; 75: 843-854. (Pubitemid 24014542)
20. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A et al. RAS is regulated by the let-7 microRNA family. Cell 2005; 120: 635-647. (Pubitemid 40343076)
21. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403: 901-906. (Pubitemid 30130993)
22. Miao H, Wei BR, Peehl DM, Li Q, Alexandrou T, Schelling JR et al. Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat cell Biol 2001; 3: 527-530. (Pubitemid 32422092)
23. Nasreen N, Mohammed KA, Antony VB. Silencing the receptor EphA2 suppresses the growth and haptotaxis of malignant mesothelioma cells. Cancer 2006; 107: 2425-2435. (Pubitemid 44748526)
24. Fuentes-Calvo I, Blazquez-Medela AM, Santos E, Lopez-Novoa JM, Martinez-Salgado C. Analysis of k-ras nuclear expression in fibroblasts and mesangial cells. PloS one 2010; 5: e8703.
25. Hutvagner G, Simard MJ, Mello CC, Zamore PD. Sequencespecific inhibition of small RNA function. PLoS Biol 2004; 2: E98.
26. Bao S, Wang Y, Sweeney P, Chaudhuri A, Doseff AI, Marsh CB et al. Keratinocyte growth factor induces Akt kinase activity and inhibits Fas-mediated apoptosis in A549 lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2005; 288: L36-L42. (Pubitemid 40023884)
27. Nasreen N, Mohammed KA, Mubarak KK, Baz MA, Akindipe OA, Fernandez-Bussy S et al. Pleural mesothelial cell transformation into myofibroblasts and haptotactic migration in response to TGF-beta1 in vitro. Am J Physiol Lung Cell Mol Physiol 2009; 297: L115-L124.
28. de Planell-Saguer M, Rodicio MC, Mourelatos Z. Rapid in situ codetection of noncoding RNAs and proteins in cells and formalin-fixed paraffin-embedded tissue sections without protease treatment. Nat Protoc 2010; 5: 1061-1073.
29. Pass HI, Vogelzang N, Hahn S, Carbone M. Malignant pleural mesothelioma. Curr Probl Cancer 2004; 28: 93-174. (Pubitemid 38747012)
30. Noblitt LW, Bangari DS, Shukla S, Mohammed S, Mittal SK. Immunocompetent mouse model of breast cancer for preclinical testing of EphA2-targeted therapy. Cancer Gene Ther 2005; 12: 46-53. (Pubitemid 39665242)
31. Wohlfahrt JG, Karagiannidis C, Kunzmann S, Epstein MM, Kempf W, Blaser K et al. Ephrin-A1 suppresses Th2 cell activation and provides a regulatory link to lung epithelial cells. J Immunol 2004; 172: 843-850. (Pubitemid 38113740)
32. Wykosky J, Gibo DM, Debinski W. A novel, potent, and specific ephrinA1-based cytotoxin against EphA2 receptor expressing tumor cells. Mol Cancer Therap 2007; 6: 3208-3218.
33. Thirkettle I, Harvey P, Hasleton PS, Ball RY, Warn RM. Immunoreactivity for cadherins, HGF/SF, met, and erbB-2 in pleural malignant mesotheliomas. Histopathology 2000; 36: 522-528. (Pubitemid 30348777)
34. Pass HI, Robinson BW, Testa JR, Carbone M. Emerging translational therapies for mesothelioma. Chest 1999; 116: 455S-460S. (Pubitemid 30013156)
35. Barsky SH, Roth MD, Kleerup EC, Simmons M, Tashkin DP. Histopathologic and molecular alterations in bronchial epithelium in habitual smokers of marijuana, cocaine, and/or tobacco. J Natl Cancer Inst 1998; 90: 1198-1205. (Pubitemid 28407085)
36. Chin LJ, Ratner E, Leng S, Zhai R, Nallur S, Babar I et al. A SNP in a let-7 microRNA complementary site in the KRAS untranslated region increases non-small cell lung cancer risk. Cancer Res 2008; 68: 8535-8540.
37. Brannan JM, Dong W, Prudkin L, Behrens C, Lotan R, Bekele BN et al. Expression of the receptor tyrosine kinase EphA2 is increased in smokers and predicts poor survival in non-small cell lung cancer. Clin Cancer Res 2009; 15: 4423-4430.
38. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006; 9: 189-198. (Pubitemid 43357945)
39. Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D et al. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res 2007; 67: 7713-7722. (Pubitemid 47281364)
40. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004; 64: 3753-3756. (Pubitemid 38697282)
41. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG et al. CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma-a miRNA microarray analysis. Genes Chrom Cancer 2009; 48: 615-623.
42. Schultz J, Lorenz P, Gross G, Ibrahim S, Kunz M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorageindependent growth. Cell Res 2008; 18: 549-557. (Pubitemid 351630945)
43. Akao Y, Nakagawa Y, Naoe T. Let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol Pharmaceut Bull 2006; 29: 903-906.
44. Kumar MS, Erkeland SJ, Pester RE, Chen CY, Ebert MS, Sharp PA et al. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci USA 2008; 105: 3903-3908. (Pubitemid 351723497)
45. Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 2007; 21: 1025-1030. (Pubitemid 46686471)
46. Eder M, Scherr M. MicroRNA and lung cancer. N Engl J Med 2005; 352: 2446-2448. (Pubitemid 40958446)