Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells

Nature

Volumn 497, Issue 7451, 2013, Pages 633-637

  Commisso, Cosimo ^a   Davidson, Shawn M ^b   Soydaner Azeloglu, Rengin G ^a   Parker, Seth J ^c   Kamphorst, Jurre J ^d   Hackett, Sean ^d   Grabocka, Elda ^a   Nofal, Michel ^d   Drebin, Jeffrey A ^e   Thompson, Craig B ^f   Rabinowitz, Joshua D ^d   Metallo, Christian M ^c   Vander Heiden, Matthew G ^b,g   Bar Sagi, Dafna ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d PRINCETON UNIVERSITY   (United States)

^e HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBON; CELL PROTEIN; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; GLUTAMINE; RAS PROTEIN;

AMINO ACID; BIOLOGICAL UPTAKE; CARBON; CELL ORGANELLE; EXPLOITATION; GROWTH RATE; INHIBITION; METABOLISM; PHENOTYPE; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBON METABOLISM; CELL GROWTH; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; MOUSE; NONHUMAN; NUTRIENT UPTAKE; PANCREAS TUMOR; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TRANSPORT; TUMOR XENOGRAFT;

AMINO ACIDS; ANIMALS; BIOLOGICAL TRANSPORT; CARBON; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; FEMALE; GLUTAMINE; MICE; MICE, NUDE; NIH 3T3 CELLS; ONCOGENE PROTEIN P21(RAS); PANCREATIC NEOPLASMS; PINOCYTOSIS; PROTEOLYSIS;

EID: 84878396462     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12138     Document Type: Article

References (31)

1. Bar-Sagi, D. & Feramisco, J. R. Induction ofmembrane ruffling and fluid-phase pinocytosis in quiescent fibroblastsby rasproteins. Science 233, 1061-1068(1986).
2. Porat-Shliom, N., Kloog, Y.&Donaldson, J. G.A unique platformfor H-Ras signaling involving clathrin-independent endocytosis. Mol. Biol. Cell 19, 765-775 (2008).
3. Walsh, A. B.&Bar-Sagi, D. Differential activation of the Rac pathway by Ha-Ras and K-Ras. J. Biol. Chem. 276, 15609-15615 (2001).
4. Lopez-Crapez, E., Chypre, C., Saavedra, J., Marchand, J. & Grenier, J. Rapid and large-scale method to detect K-ras gene mutations in tumor samples. Clin. Chem. 43, 936-942 (1997).
5. Aoki, K., Yoshida, T., Sugimura, T. & Terada, M. Liposome-mediated in vivo gene transfer of antisense K-ras construct inhibits pancreatic tumor dissemination in the murine peritoneal cavity. Cancer Res. 55, 3810-3816 (1995).
6. Ivanov, A. I.Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? Methods Mol. Biol. 440, 15-33 (2008).
7. West, M. A., Bretscher, M. S.&Watts, C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J. Cell Biol. 109, 2731-2739 (1989).
8. Capon, D. J., Chen, E. Y., Levinson, A. D., Seeburg, P. H. & Goeddel, D. V. Complete nucleotide sequences of the T24 human bladder carcinoma oncogene and its normal homologue. Nature 302, 33-37 (1983).
9. Knowles, M. A. & Williamson, M. Mutation of H-ras is infrequent in bladder cancer: confirmation by single-strand conformation polymorphism analysis, designed restriction fragment length polymorphisms, and direct sequencing. Cancer Res. 53, 133-139 (1993).
10. Wagner, M. et al. A murine tumor progression model for pancreatic cancer recapitulating the genetic alterations of the human disease. Genes Dev. 15, 286-293 (2001).
11. Hingorani, S. R. et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7, 469-483 (2005).
12. Nolan-Stevaux, O. et al. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev. 23, 24-36 (2009).
13. Stehle, G. et al. Plasma protein (albumin) catabolism by the tumor itself-implications for tumor metabolism and the genesis of cachexia. Crit. Rev. Oncol. Hematol. 26, 77-100 (1997).
14. Gaglio, D., Soldati, C., Vanoni, M., Alberghina, L. & Chiaradonna, F. Glutamine deprivation induces abortive s-phase rescued by deoxyribonucleotides in k-ras transformed fibroblasts. PLoS ONE 4, e4715 (2009).
15. Matés, J. M. et al. Glutamine homeostasis and mitochondrial dynamics. Int. J. Biochem. Cell Biol. 41, 2051-2061 (2009).
16. Reis, R. C., Sorgine, M. H. & Coelho-Sampaio, T. A novel methodology for the investigation of intracellular proteolytic processing in intact cells. Eur. J. Cell Biol. 75, 192-197 (1998).
17. Newsholme, E. A., Crabtree, B. & Ardawi, M. S. Glutamine metabolism in lymphocytes: its biochemical, physiological and clinical importance. Q. J. Exp. Physiol. 70, 473-489 (1985).
18. Wu, M. C., Arimura, G. K. & Yunis, A. A. Mechanism of sensitivity of cultured pancreatic carcinoma to asparaginase. Int. J. Cancer 22, 728-733 (1978).
19. Gaglio, D. et al. Oncogenic K-Ras decouples glucose and glutamine metabolism to support cancer cell growth. Mol. Syst. Biol. 7, 523 (2011).
20. Metallo, C. M. et al.Reductive glutaminemetabolismby IDH1mediates lipogenesis under hypoxia. Nature 481, 380-384 (2012).
21. Hirai, H. & Varmus, H. E. SH2 mutants of c-src that are host-dependent for transformation are transdominant inhibitors of mouse-cell transformation by activated c-src. Genes Dev. 4, 2342-2352 (1990).
22. Kasahara, K. et al. Role of Src-family kinases in formation and trafficking of macropinosomes. J. Cell. Physiol. 211, 220-232 (2007).
23. Mettlen, M. et al. Src triggers circular ruffling and macropinocytosis at the apical surface of polarized MDCK cells. Traffic 7, 589-603 (2006).
24. Veithen, A., Cupers, P., Baudhuin, P. & Courtoy, P. J. v-Src induces constitutive macropinocytosis in rat fibroblasts. J. Cell Sci. 109, 2005-2012 (1996).
25. Bos, J. L. ras oncogenes in human cancer: a review. Cancer Res. 49, 4682-4689 (1989).
26. Jones, S. et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321, 1801-1806 (2008).
27. Holm, E. et al. Substrate balances across colonic carcinomas in humans. Cancer Res. 55, 1373-1378 (1995).
28. Tsakraklides, V. & Bell, S. P. Dynamics of pre-replicative complex assembly. J. Biol. Chem. 285, 9437-9443 (2010).
29. Wise, D. R. et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl Acad. Sci. USA 105, 18782-18787 (2008).
30. Antoniewicz, M. R., Kelleher, J. K. & Stephanopoulos, G. Accurate assessment of amino acid mass isotopomer distributions for metabolic flux analysis. Anal. Chem. 79, 7554-7559 (2007).
31. Fernandez, C. A., Des Rosiers, C., Previs, S. F., David, F. & Brunengraber, H. Correction of 13C mass isotopomer distributions for natural stable isotope abundance. J. Mass Spectrom. 31, 255-262 (1996).