Noncanonical roles of membranous lysyl-tRNA synthetase in transducing cell-substrate signaling for invasive dissemination of colon cancer spheroids in 3D collagen I gels

Oncotarget

Volumn 6, Issue 25, 2015, Pages 21655-21674

  Nam, Seo Hee ^a   Kim, Doyeun ^a   Lee, Mi Sook ^a   Lee, Doohyung ^a   Kwak, Tae Kyoung ^a   Kang, Minkyung ^a   Ryu, Jihye ^a   Kim, Hye Jin ^a   Song, Haeng Eun ^a   Choi, Jungeun ^a   Lee, Gyu Ho ^a   Kim, Sang Yeob ^b   Park, Song Hwa ^a   Kim, Dae Gyu ^a   Kwon, Nam Hoon ^a   Kim, Tai Young ^a   Thiery, Jean Paul ^c,d,e   Kim, Sunghoon ^a   Lee, Jung Weon ^a  

^a Seoul National University   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

3D culture; Cancer metastasis; Cell ECM adhesion; Lysyl tRNA synthetase; Signal transduction

Indexed keywords

COLLAGEN GEL; INTEGRIN; LYSINE TRANSFER RNA LIGASE; MITOGEN ACTIVATED PROTEIN KINASE; PAXILLIN; PROTEIN C JUN; THREE DIMENSIONAL COLLAGEN I GEL; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; COLLAGEN TYPE 1;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL MOTION; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; METASTASIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR SPHEROID; ANIMAL; COLON TUMOR; CYTOSOL; ENZYMOLOGY; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HCT 116 CELL LINE; INDIRECT FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROTEIN SYNTHESIS; TUMOR CELL LINE;

ANIMALS; CADHERINS; CELL ADHESION; CELL LINE, TUMOR; COLLAGEN TYPE I; COLONIC NEOPLASMS; CYTOSOL; EXTRACELLULAR MATRIX; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HCT116 CELLS; HUMANS; LYSINE-TRNA LIGASE; MICE; NEOPLASM METASTASIS; PAXILLIN; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; SIGNAL TRANSDUCTION;

EID: 84940750377     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4130     Document Type: Article

References (29)

1. Thiery JP and Lim CT. Tumor Dissemination: An EMT Affair. Cancer Cell. 2013; 23:272-273.
2. Meng F and Wu G. The rejuvenated scenario of epithelial-mesenchymal transition (EMT) and cancer metastasis. Cancer Metastasis Rev. 2012; 31:455-467.
3. Kim S, You S and Hwang D. Aminoacyl-tRNA synthetases and tumorigenesis: more than housekeeping. Nat Rev Cancer. 2011; 11:708-718.
4. Park SG, Kim HJ, Min YH, Choi EC, Shin YK, Park BJ, Lee SW and Kim S. Human lysyl-tRNA synthetase is secreted to trigger proinflammatory response. Proc Natl Acad Sci U S A. 2005; 102:6356-6361.
5. Yannay-Cohen N, Carmi-Levy I, Kay G, Yang CM, Han JM, Kemeny DM, Kim S, Nechushtan H and Razin E. LysRS serves as a key signaling molecule in the immune response by regulating gene expression. Mol Cell. 2009; 34:603-611.
6. Kim DG, Choi JW, Lee JY, Kim H, Oh YS, Lee JW, Tak YK, Song JM, Razin E, Yun SH and Kim S. Interaction of two translational components, lysyl-tRNA synthetase and p40/37LRP, in plasma membrane promotes laminin-dependent cell migration. FASEB J. 2012; 26:4142-4159.
7. Kim DG, Lee JY, Kwon NH, Fang P, Zhang Q, Wang J, Young NL, Guo M, Cho HY, Mushtaq AU, Jeon YH, Choi JW, Han JM, Kang HW, Joo JE, Hur Y, et al. Chemical inhibition of prometastatic lysyl-tRNA synthetase-laminin receptor interaction. Nat Chem Biol. 2014; 10:29-34.
8. Canfield SM and Khakoo AY. The nonintegrin laminin binding protein (p67 LBP) is expressed on a subset of activated human T lymphocytes and, together with the integrin very late activation antigen-6, mediates avid cellular adherence to laminin. J Immunol. 1999; 163:3430-3440.
9. Ardini E, Tagliabue E, Magnifico A, Buto S, Castronovo V, Colnaghi MI and Menard S. Co-regulation and physical association of the 67-kDa monomeric laminin receptor and the a6β4 integrin. J Biol Chem. 1997; 272:2342-2345.
10. Berno V, Porrini D, Castiglioni F, Campiglio M, Casalini P, Pupa SM, Balsari A, Menard S and Tagliabue E. The 67 kDa laminin receptor increases tumor aggressiveness by remodeling laminin-1. Endocr Relat Cancer. 2005; 12:393-406.
11. Lee JW and Juliano R. Mitogenic signal transduction by integrin-and growth factor receptor-mediated pathways. Mol Cells. 2004; 17:188-202.
12. Jung O, Choi S, Jang SB, Lee SA, Lim ST, Choi YJ, Kim HJ, Kim DH, Kwak TK, Kim H, Kang M, Lee MS, Park SY, Ryu J, Jeong D, Cheong HK, et al. Tetraspan TM4SF5-dependent direct activation of FAK and metastatic potential of hepatocarcinoma cells. J Cell Sci. 2012; 125:5960-5973.
13. Rowe RG and Weiss SJ. Navigating ECM barriers at the invasive front: the cancer cell-stroma interface. Annu Rev Cell Dev Biol. 2009; 25:567-595.
14. Thiery JP. Metastasis: Alone or Together? Current Biology. 2009; 19:R1121-R1123.
15. Friedl P, Locker J, Sahai E and Segall JE. Classifying collective cancer cell invasion. Nat Cell Biol. 2012; 14:777-783.
16. Chua KN, Poon KL, Lim J, Sim WJ, Huang RY and Thiery JP. Target cell movement in tumor and cardiovascular diseases based on the epithelial-mesenchymal transition concept. Adv Drug Deliv Rev. 2011; 63:558-567.
17. Huang RY, Wong MK, Tan TZ, Kuay KT, Ng AH, Chung VY, Chu YS, Matsumura N, Lai HC, Lee YF, Sim WJ, Chai C, Pietschmann E, Mori S, Low JJ, Choolani M, et al. An EMT spectrum defines an anoikis-resistant and spheroidogenic intermediate mesenchymal state that is sensitive to e-cadherin restoration by a src-kinase inhibitor, saracatinib (AZD0530). Cell Death Dis. 2013; 4:e915.
18. Dumbauld DW, Lee TT, Singh A, Scrimgeour J, Gersbach CA, Zamir EA, Fu J, Chen CS, Curtis JE, Craig SW and García AJ. How vinculin regulates force transmission. Proceedings of the National Academy of Sciences. 2013; 110:9788-9793.
19. Clark K, Howe JD, Pullar CE, Green JA, Artym VV, Yamada KM and Critchley DR. Tensin 2 modulates cell contractility in 3D collagen gels through the RhoGAP DLC1. J Cell Biochem. 2010; 109:808-817.
20. Hoj JP, Davis JA, Fullmer KE, Morrell DJ, Saguibo NE, Schuler JT, Tuttle KJ and Hansen MDH. Cellular contractility changes are sufficient to drive epithelial scattering. Exp Cell Res. 2014; 326:187-200.
21. Katoh K, Masuda M, Kano Y, Jinguji Y and Fujiwara K. Focal adhesion proteins associated with apical stress fibers of human fibroblasts. Cell Motility & the Cytoskeleton. 1995; 31:177-195.
22. Bellis SL, Miller JT and Turner CE. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J Biol Chem. 1995; 270:17437-17441.
23. Guller MC, Andre J, Legrand A, Setterblad N, Mauviel A, Verrecchia F, Daniel F and Bernuau D. c-Fos accelerates hepatocyte conversion to a fibroblastoid phenotype through ERK-mediated upregulation of paxillin-Serine178 phosphorylation. Mol Carcinog. 2009; 48:532-544.
24. Wary KK, Mariotti A, Zurzolo C and Giancotti FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell. 1998; 94:625-634.
25. Lu KK, Armstrong SE, Ginnan R and Singer HA. Adhesion-dependent activation of CaMKII and regulation of ERK activation in vascular smooth muscle. Am J Physiol Cell Physiol. 2005; 289:C1343-1350.
26. Lee MS, Kim S, Kim BG, Won C, Nam SH, Kang S, Kim HJ, Kang M, Ryu J, Song HE, Lee D, Ye SK, Jeon NL, Kim TY, Cho NH and Lee JW. Snail1 induced in breast cancer cells in 3D collagen I gel environment suppresses cortactin and impairs effective invadopodia formation. Biochim Biophys Acta. 2014; 1843:2037-2054.
27. Lee SA, Kim YM, Kwak TK, Kim HJ, Kim S, Kim SH, Park KH, Cho M and Lee JW. The extracellular loop 2 of TM4SF5 inhibits integrin α2 on hepatocytes under collagen type I environment. Carcinogenesis. 2009; 30:1872-1879.
28. Harvey CD, Ehrhardt AG, Cellurale C, Zhong H, Yasuda R, Davis RJ and Svoboda K. A genetically encoded fluorescent sensor of ERK activity. Proc Natl Acad Sci USA. 2008; 105:19264-19269.
29. Lim S-T, Chen XL, Lim Y, Hanson DA, Vo T-T, Howerton K, Larocque N, Fisher SJ, Schlaepfer DD and Ilic D. Nuclear FAK Promotes Cell Proliferation and Survival through FERM-Enhanced p53 Degradation. Molecular Cell. 2008; 29:9-22.