Arginine deprivation affects glioblastoma cell adhesion, invasiveness and actin cytoskeleton organization by impairment of β-actin arginylation

Amino Acids

Volumn 47, Issue 1, 2015, Pages 199-212

  Pavlyk, Iuliia ^a   Rzhepetskyy, Yuriy ^b   Jagielski, Adam K ^c   Drozak, Jakub ^c   Wasik, Anna ^a   Pereverzieva, Galyna ^b   Olchowik, Marta ^a   Kunz Schugart, Leoni A ^d   Stasyk, Oleh ^b   Redowicz, Maria Jolanta ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b INSTITUTE OF CELL BIOLOGY   (Ukraine)

^c UNIVERSITY OF WARSAW   (Poland)

^d UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

Actin arginylation; Actin cytoskeleton; Amino acid deprivation; Cancer; Cell migration; Invasiveness

Indexed keywords

ARGININE; BETA ACTIN; BETA TUBULIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HERMES ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; TALIN; UVOMORULIN; VINCULIN; ACTIN;

ACTIN FILAMENT; ADULT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARGINYLATION; ARTICLE; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; FEMALE; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; RAT; BRAIN TUMOR; CYTOSKELETON; GLIOBLASTOMA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; TUMOR CELL LINE; TUMOR INVASION;

ACTIN CYTOSKELETON; ACTINS; ARGININE; BRAIN NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CYTOSKELETON; GLIOBLASTOMA; HUMANS; NEOPLASM INVASIVENESS;

EID: 84947922181     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-014-1857-1     Document Type: Article

References (45)

1. Agrawal V, Alpini SE, Stone EM, Frenkel EP, Frankel AE (2012) Targeting methionine auxotrophy in cancer: Discovery and exploration. Expert Opin Biol Ther 12:53-61
2. Albini A, Iwamoto Y, Kleinman HK, Martin GR, Aaronson SA, Kozlowski JM, McEwan RN (1987) A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 47:3239-3245
3. Allen PG, Shuster CB, Käs J, Chaponnier C, Janmey PA, Herman IM (1996) Phalloidin binding and rheological differences among actin isoforms. Biochemistry 35:14062-14069
4. Allen MD, Luong P, Hudson C et al (2014) Prognostic and therapeutic impact of argininosuccinate synthetase 1 control in bladder cancer as monitored longitudinally by PET imaging. Cancer Res 74:896-907
5. Bobak YP, Vynnytska BO, Kurlishchuk YV, Sibirny AA, Stasyk OV (2010) Cancer cell sensitivity to arginine deprivation in vitro is not determined by endogenous levels of arginine metabolic enzymes. Cell Biol Int 34:1085-1089
6. Bowles TL, Kim R, Galante J, Parsons CM, Virudachalam S, Kung HJ, Bold RJ (2008) Pancreatic cancer cell lines deficient in argininosuccinate synthetase are sensitive to arginine deprivation by arginine deiminase. Int J Cancer 123:1950-1955
7. Brandes AA (2007) State-of-the-art treatment of high-grade brain tumors. Semin Oncol 30(Suppl 19):4-9
8. Bregier C, Krzemień-Ojak L, Włoga D et al (2013) PHLP2 is essential and plays a role in ciliogenesis and microtubule assembly in Tetrahymena thermophila. J Cell Physiol 228:2175-2189
9. Choi BS, Martinez-Falero IC, Corset C, Munder M, Modolell M, Müller I, Kropf P (2009) Differential impact of l-arginine deprivation on the activation and effector functions of T cells and macrophages. J Leukoc Biol 85:268-277
10. Covini D, Tardito S, Bussolati O, Chiarelli LR, Pasquetto MV, Digilio R, Valentini G, Scotti C (2012) Expanding targets for a metabolic therapy of cancer: l-asparaginase. Recent Pat Anticancer Drug Discov 7:4-13
11. Delage B, Fennell DA, Nicholson L, McNeish I, Lemoine NR, Crook T, Szlosarek PW (2010) Arginine deprivation and argininosuccinate synthetase expression in the treatment of cancer. Int J Cancer 126:2762-2772
12. Dillon BJ, Prieto VG, Curley SA, Ensor CM, Holtsberg FW, Bomalaski JS, Clark MA (2004) Incidence and distribution of argininosuccinate synthetase deficiency in human cancers: A method for identifying cancers sensitive to arginine deprivation. Cancer 100:826-833
13. Drozak J, Chrobok L, Poleszak O, Jagielski AK, Derlacz R (2013) Molecular identification of carnosine N-methyltransferase as chicken histamine N-methyltransferase-like protein (hnmt-like). PLoS ONE 8:e64805
14. Feun L, You M, Wu CJ, Kuo MT, Wangpaichitr M, Spector S, Savaraj N (2008) Arginine deprivation as a targeted therapy for cancer. Curr Pharm Des 14:1049-1057
15. Glazer ES, Piccirillo M, Albino V et al (2010) Phase II study of pegylated arginine deiminase for nonresectable and metastatic hepatocellular carcinoma. J Clin Oncol 28:2220-2226
16. Hlavaty J, Jandl G, Liszt M, Petznek H, König-Schuster M, Sedlak J, Egerbacher M, Weissenberger J, Salmons B, Günzburg WH, Renner M (2011) Comparative evaluation of preclinical in vivo models for the assessment of replicating retroviral vectors for the treatment of glioblastoma. J Neurooncol 102:59-69
17. Karakozova M, Kozak M, Wong CC et al (2006) Arginylation of β-actin regulates actin cytoskeleton and cell motility. Science 313:192-196
18. Kim RH, Coates JM, Bowles TL et al (2009) Arginine deiminase as a novel therapy for prostate cancer induces autophagy and caspase-independent apoptosis. Cancer Res 69:700-708
19. Kouvroukoglou S, Dee KC, Bizios R, McIntire LV, Zygourakis K (2000) Endothelial cell migration on surfaces modified with immobilized adhesive peptides. Biomaterials 21:1725-1733
20. Kurosaka S, Leu NA, Pavlov I et al (2012) Arginylation regulates myofibrils to maintain heart function and prevent dilated cardiomyopathy. J Mol Cell Cardiol 53:333-341
21. Majewski L, Sobczak M, Wasik A, Skowronek K, Rędowicz MJ (2011) Myosin VI in PC12 cells play important roles in cell migration and proliferation but not in catecholamine secretion. J Muscle Res Cell Motil 32:291-302
22. Morris SM (2007) Arginine metabolism: boundaries of our knowledge. J Nutr 137(Suppl 2):1602S-1609S
23. Morrow K, Hernandez CP, Raber P et al (2013) Anti-leukemic mechanisms of pegylated arginase I in acute lymphoblastic T-cell leukemia. Leukemia 27:569-577
24. Peickert S, Waurig J, Dittfeld C et al (2012) Rapid re-expression of CD133 protein in colorectal cancer cell lines in vitro and in vivo. Lab Invest 92:1607-1622
25. Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326:1208-1212
26. Saha S, Mundia MM, Zhang F et al (2010) Arginylation regulates intracellular actin polymer level by modulating actin properties and binding of capping and severing proteins. Mol Biol Cell 21:1350-1361
27. Saha S, Wang J, Buckley B, Wang Q, Lilly B, Chernov M, Kashina A (2012) Small molecule inhibitors of arginyltransferase regulate arginylation-dependent protein degradation, cell motility, and angiogenesis. Biochem Pharmacol 83:866-873
28. Scott L, Lamb J, Smith S, Wheatley DN (2000) Single amino acid (arginine) deprivation: Rapid and selective death of cultured transformed and malignant cells. Br J Cancer 83:800-810
29. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850-858
30. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protocol 1:2856-2860
31. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182
32. Syed N, Langer J, Janczar K et al (2013) Epigenetic status of argininosuccinate synthetase and argininosuccinate lyase modulates autophagy and cell death in glioblastoma. Cell Death Dis 4:e458
33. Terman JR, Kashina A (2013) Post-translational modification and regulation of actin. Curr Opin Cell Biol 25:30-38
34. Tönjes M, Barbus S, Park YJ et al (2013) BCAT1 promotes cell proliferation through amino acid catabolism in gliomas carrying wild-type IDH1. Nat Med 19:901-908
35. Vynnytska-Myronovska B, Bobak Y, Garbe Y, Dittfeld C, Stasyk O, Kunz-Schughart LA (2012) Single amino acid arginine starvation efficiently sensitizes cancer cells to canavanine treatment and irradiation. Int J Cancer 130:2164-2175
36. Wheatley DN (2004) Controlling cancer by restricting arginine availability - arginine-catabolizing enzymes as anticancer agents. Anticancer Drugs 15:825-833
37. Wheatley DN, Kilfeather R, Stitt A, Campbell E (2005) Integrity and stability of the citrulline-arginine pathway in normal and tumour cell lines. Cancer Lett 227:141-152
38. Wong CC, Xu T, Rai R, Bailey AO, Yates JR 3rd, Wolf YI, Zebroski H, Kashina A (2007) Global analysis of posttranslational protein arginylation. PLoS Biol 5:e258
39. Yang TS, Lu SN, Chao Y et al (2010) A randomised phase II study of pegylated arginine deiminase (ADI-PEG 20) in Asian advanced hepatocellular carcinoma patients. Br J Cancer 103:954-960
40. Yau T, Cheng PN, Chan P, Chan W, Chen L, Yuen J, Pang R, Fan ST, Poon RT (2013) Aphase 1 dose-escalating study of pegylated recombinant human arginase 1 (Peg-rhArg1) in patients with advanced hepatocellular carcinoma. Invest NewDrugs 31:99-107
41. Yi J, Horky LL, Friedlich AL, Shi Y, Rogers JT, Huang X (2009) l-arginine and Alzheimer's disease. Int J Clin Exp Pathol 2:211-238
42. Yoon CY, Shim YJ, Kim EH, Lee JH, Won NH, Kim JH, Park IS, Yoon DK, Min BH (2007) Renal cell carcinoma does not express argininosuccinate synthetase and is highly sensitive to arginine deprivation via arginine deiminase. Int J Cancer 20:897-905
43. Yoon JK, Frankel AE, Feun LG, Ekmekcioglu S, Kim KB (2013) Arginine deprivation therapy for malignant melanoma. Clin Pharmacol 5:11-19
44. Zawadzka M, Kaminska B (2003) Immunosuppressant FK506 affects multiple signaling pathways and modulates gene expression in astrocytes. Mol Cell Neurosci 22:202-209
45. Zhang F, Saha S, Kashina A (2012) Arginylation-dependent regulation of a proteolytic product of talin is essential for cell-cell adhesion. J Cell Biol 197:819-836