Selective amino acid restriction targets mitochondria to induce apoptosis of androgen-independent prostate cancer cells

Journal of Cellular Physiology

Volumn 209, Issue 2, 2006, Pages 522-534

  Fu, Ya Min ^a   Zhang, Hui ^a   Ding, Mingjie ^a   Li, Yi Qi ^a   Fu, Xing ^a   Yu, Zu Xi ^b   Meadows, Gary G ^a,b  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; ANDROGEN; APOPTOSIS INDUCING FACTOR; CASPASE; GLUTAMINE; METHIONINE; MITOCHONDRIAL PROTEIN; PHENYLALANINE; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; RAF PROTEIN; REACTIVE OXYGEN METABOLITE; TYROSINE;

AMINO ACID RESTRICTION; AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CANCER CELL; CELL DAMAGE; CELL FUNCTION; CELL LINE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENERGY YIELD; ENZYME ACTIVITY; ENZYME INDUCTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; AMINO ACIDS; ANDROGENS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASES; ENZYME ACTIVATION; HUMANS; MALE; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RAF KINASES; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED;

EID: 33749253359     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20766     Document Type: Article

References (78)

1. 2-terminal kinase. J Cell Biol 149:741-754.
2. 2-terminal kinase/activator protein 1 pathway an inhibition of extracellular signal-regulated kinase are early effects in paclitaxel-mediated apoptosis in human B lymphoblasts. Cancer Res 58:241-247.
3. Ballif AB, Blenis J. 2001. Molecular mechanisms mediating mammalian mitogen-activate protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ 12:397-408.
4. Barboule N, Truchet I, Valette A. 2005. Localization of phosphorylated forms of Bcl-2 in mitosis: Co-localization with Ki-67 and nucleolin in nuclear structures and on mitotic chromosomes. Cell Cycle 4:590-596.
5. Blagosklonny MV, Schulte T, Nguyen P, Trepel J, Neckers LM. 1996. Taxol-induced apoptosis and phosphorylation of Bcl-2 protein involves c-Raf-1 and represents a novel c-Raf-1 signal transduction pathway. Cancer Res 56:1851-1854.
6. Boise LH, Gonz'alez-Garc'ia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thompson CB. 1993. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608.
7. Chen X, Thakkar H, Tyan F, Gim S, Robinson H, Lee C, Pandey SK, Nwokorie C, Onwudiwe N, Srivastava RK. 2001. Constitutively active Akt is an important regulator of TRAIL sensitivity in prostate cancer. Oncogene 20:6073-6083.
8. Clarke MF, Apel IJ, Benedict MA, Eipers PG, Sumantran V, Doedens M, Fukunaga N, Davidson B, Dick JE, Minn AJ, Boise LH, Thompson CB, Wicha M, Nunez G. 1995. A recombinant bcl-xs adenovirus selectively induces apoptosis in cancer cells but not in normal bone marrow cells. Proc Natl Acad Sci 92:11024-11028.
9. Conlon I, Raff M. 1999. Size control in animal development. Cell 96:235-244.
10. Cristofano AD, Pandolfi PP. 2000. The multiple roles of PTEN in tumor suppression. Cell 100:387-390.
11. Denmeade SR, Isaacs JT. 1996. Activation of programmed (apoptotic) cell death for the treatment of prostate cancer. In: August JT, Anders MW, Murad F, Coyle JT, editors. Advances in pharmacology, Vol. 35, San Diego: Academic Press, pp 281-305.
12. Du K, Herzig S, Kulkarni RN, Montminy M. 2003. TRB3: A tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300:1574-1577.
13. Elstad CA, Meadows GG. 1993. Modulation of B16-BL6 murine melanoma metastatic phenotype by tyrosine and phenylalanine restriction in the absence of host selection pressures. Anticancer Res 13:523-528.
14. Epner DE. 2001. Can dietary methionine restriction increase the effectiveness of chemotherapy in treatment of advanced cancer? J Am Coll Nutr 5:443S-475S.
15. Epner DE, Morrow S, Wilcox M, Houghton JL. 2002. Nutrient intake and nutritional indexes in adults with metastatic cancer on a phase I clinical trial of dietary methionine restriction. Nutr Cancer 42:158-166.
16. Frisch SM, Vuori K, Ruoslahti E, Chan-Hui P-Y. 1996. Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 134:793-799.
17. Fu Y-M, Yu Z-X, Ferrans VJ, Meadows GG. 1997. Tyrosine and phenylalanine restriction induces G0/G1 cell cycle arrest in murine melanoma in vitro and in vivo. Nutr Cancer 29:104-113.
18. Fu Y-M, Yu Z-X, Pelayo BA, Ferrans VJ, Meadows GG. 1999. Focal adhesion kinase-dependent apoptosis of melanoma induced by tyrosine and phenylalanine deficiency. Cancer Res 59:758-765.
19. Fu Y-M, Yu ZX, Li Y-Q, Ge X, Sanchez PJ, Fu X, Meadows GG. 2003. Specific amino acid dependency regulates invasiveness and viability of androgen-independent prostate cancer cells. Nutr Cancer 45:60-73.
20. Fu YM, Zhang H, Ding M, Li YQ, Fu X, Yu ZX, Meadows GG. 2004. Specific amino acid restriction inhibits attachment and spreading of human melanoma via modulation of the integrin/focal adhesion kinase pathway and actin cytoskeleton remodeling. Clin Exp Metastasis 21:587-598.
21. Gajewski TF, Thompson CB. 1996. Apoptosis meets signal transduction: Elimination of a BAD influence. Cell 87:589-592.
22. Ge X, Fu Y-M, Li Y-Q, Meadows GG. 2002. Activation of caspases and cleavage of Bid are required for tyrosine and phenylalanine deficiency-induced apoptosis of human A375 melanoma cells. Arch Biochem Biophys 403:50-58.
23. Gilmore AP, Metcalfe AD, Romer LH, Streuli CH. 2000. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J Cell Biol 149:431-445.
24. Green DR, Evans GI. 2002. A matter of life and death. Cancer Cell 1:19-30.
25. Gross A, McDonnell J, Korsmeyer S. 1999. BCL-2 family members and the mitochondria in apoptosis. Gene Dev 13:1899-1911.
26. Gupta A, Miki K, Xu M, Yamamoto N, Moosa AR, Hoffman RM. 2003. Combination efficacy of doxorubicin and adenoviral methioninase gene therapy with prodrug selenomethionine. Anticancer Res 2B:1181-1188.
27. Haldar S, Jena N, Croce CM. 1995. Inactivation of Bcl-2 by phosphorylation. Proc Nat Acad Sci 92:4507-4511.
28. Hockenbery DM, Oltvai ZN, Yin X-M, Millman CL, Korsmeyer SJ. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-251.
29. Hoetelmans R, van Slooten HJ, Keijzer R, Erkeland S, van de Velde CJ, Dierendonck JH. 2000. Bcl-2 and Bax proteins are present in interphase nuclei of mammalian cells. Cell Death Differ 7:384-392.
30. FAK in cultured fibroblasts results in apoptosis. J Cell Biol 135:1383-1390.
31. Izuishi K, Kato K, Ogura T, Kinoshita T, Esumi H. 2000. Remarkable tolerance of tumor cells to nutrient deprivation: Possible new biochemical target for cancer therapy. Cancer Res 60:6201-6207.
32. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CYJ, Sasaki T, Ella AJ, Cheng H-Y, Ravagnan L, Ferri KF, Zamzami N, Wakeham A, Hakem R, Yoshida H, Kong Y, Mak TW, Zúñlga-Pflücker JC, Kroemer G, Penninger JM. 2001. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410:549-554.
33. Kawabi-Addo B, Giri D, Schmidt K, Podsypanina K, Parsons R, Greenberg N, Ittmann M. 2001. Haploinsufficiency of the Pten tumor suppressor gene promotes prostate cancer progression. Proc Natl Acad Sci 98:11563-11568.
34. Klein RD, Fischer SM. 2002. Black tea polyphenols inhibit IGF-I-induced signaling through Akt in normal prostate epithelial cells and Du145 prostate carcinoma cells. Carcinogenesis 23:217-221.
35. Kluck RM, Esposti MD, Perkins G, Renken C, Kuwana T, Bossy-Wetzel E, Goldberg M, Allen T, Barber MJ, Green DR, Newmeyer DD. 1999. The pro-apoptotic proteins Bid and Bax cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J Cell Biol 147:809-822.
36. Kokkinaki DM, Hoffman RM, Frenkel EP, Wick JB, Han Q, Xu M, Tan Y, Schold SC. 2001. Synergy between methionine stress and chemotherapy in the treatment of brain tumor xenografts in athymic mice. Cancer Res 61:4017-4023.
37. Kroemer G. 1997. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med 3:614-620.
38. Lin J, Adam RM, Santiestevan E, Freeman MR. 1999. The phosphatidylinositol 3′-kinase pathway is a dominant growth factor-activated cell survival pathway in LNCaP human prostate carcinoma cells. Cancer Res 59:2891-2897.
39. Lin B, Kolluri SK, Lin F, Liu W, Han YH, Cao X, Dawson MI, Reed JC, Zhang XK. 2004. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 116:527-540.
40. Lu S, Chen GL, Ren C, Kwabi-Addo B, Epner DE. 2003. Methionine restriction selectively targets thymidylate synthase in prostate cancer cells. Biochem Pharmacol 66:791-800.
41. Maira SM, Galetic I, Brazil DP, Kaech S, Ingley E, Thelen M, Hemmings BA. 2001. Carboxyl-terminal modulator protein (CTMP), a negative regulator of PKB/Akt and v-Akt at the plasma membrane. Science 294:374-380.
42. Massaad CA, Portier BP, Taglialatela G. 2004. Inhibition of transcription factor activity by nuclear compartment-associated Bcl-2. J Biol Chem 279:54470-54478.
43. McDonnell TJ, Meyn RE, Robertson LE. 1995. Implications of apoptotic cell death regulation in cancer therapy. Cancer Biol 6:53-60.
44. Meadows GG, DiGiovanni J, Minor L, Elmer GW. 1976. Some biological properties and an in vivo evaluation of tyrosine phenol-lyase on growth of B-16 melanoma. Cancer Res 36:167-171.
45. Miki K, Xu M, Gupta A, Ba Y, Tan Y, Al-Refaie W, Bouvet M, Makuuchi M, Moossa AR, Hoffman RM. 2001. Methioninase cancer gene therapy with selenomethionine as suicide prodrug substrate. Cancer Res 61:6805-6810.
46. Norris JR, Meadows GG, Massey LK, Starkey JR, Sylvester DM, Liu S-Y. 1990. Tyrosine- and phenylalanine-restricted formula diet augments immunocompetence in healthy humans. Am J Clin Nutr 51:188-196.
47. Parise LV, Lee JW, Juliano RL. 2000. New aspects of integrin signaling in cancer. Semin Cancer Biol 10:407-414.
48. Pelayo BA, Fu Y-M, Meadows GG. 1999. Inhibition of B16BL6 melanoma invasion by tyrosine and phenylalanine deprivation is associated with decreased secretion of plasminogen activators and increased plasminogen activator inhibitors. Clin Exp Metastasis 17:841-848.
49. Pelayo BA, Fu Y-M, Meadows GG. 2001. Decreased tissue plasminogen activator and increased plasminogen activator inhibitors are associated with inhibition of invasion in human A375 melanoma deprived of tyrosine and phenylalanine. Int J Oncol 18:877-883.
50. Persad S, Attwell S, Gray V, Delcommenne M, Troussard A, Sanghera J, Dedhar S. 2000. Inhibition of integrin-linked kinase (ILK) suppresses activation of protein kinase B/Akt and induces cell cycle arrest and apoptosis of PTEN-mutant prostate cancer cells. Proc Natl Acad Sci 97:3207-3212.
51. Poirson-Bichat F, Gonfalone G, Bras-Gonçalves RA, Dutrillaux B, Poupon MF. 1997. Growth of methionine-dependent human prostate cancer (PC-3) is inhibited by ethionine combined with methionine starvation. Br J Cancer 75:1605-1612.
52. 1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci 96:2110-2115.
53. Reed JC. 1994. Bcl-2 and regulation of programmed cell death. J Cell Biol 124:1-6.
54. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD, Glass DJ. 1999. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286:1738-1741.
55. Sedlak TW, Oltvai Z, Yang E, Wang K, Boise LH, Thompson CB, Korsmeyer SJ. 1995. Mutiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci 92:7834-7838.
56. Sellers WR, Fisher DE. 1999. Apoptosis and cancer drug targeting. J Clin Invest 104:1655-1661.
57. Shimizu S, Eguchi Y, Kamiike W, Waguri S, Uchiyama Y, Matsuda H, Tsujimoto Y. 1996. Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13:21-29.
58. Sonoda Y, Wanatabe S, Matsumoto Y, Aizu-Yokota E, Kasahara T. 1999. FAK is the upstream signal protein of the phosphatidylinositol 3-kinase-Akt survival pathway in hydrogen peroxide-induced apoptosis of a human glioblastoma cell line. J Biol Chem 274:10566-10570.
59. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Ioeffler M, Larochette N, Goodlett DR, Aebersold R, Sidervski DS, Penninger JM, Kromer G. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
60. Takayama S, Sato T, Krajewski S, Kochel K, Irie S, Millan JA, Reed JC. 1995. Cloning and functional analysis of BAG-1: A novel Bcl-2-binding protein with anti-cell death activity. Cell 80:279-284.
61. Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, Yamada M. 1998. Inhibition of cell migration spreading and focal adhesion by tumor suppressor PTEN. Science 280:1614-1617.
62. Tenniswood M. 1997. Apoptosis, tumour invasion and prostate cancer. Br J Urol 79:27-34.
63. Thornberry NA, Lazebnik Y. 1998. Caspases: Enemies within. Science 281:1312-1316.
64. Wang H-G, Miyashita T, Takayama S, Sato T, Torigoe T, Krajewski S, Tanaka S, Hovey L III, Troppmair J, Rapp UR, Reed JC. 1994. Apoptosis regulation by interaction of Bcl-2 protein and Raf-1 kinase. Oncogene 9:2751-2756.
65. Wang HG, Rapp UR, Reed JC. 1996. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87:629-638.
66. Wang X, Yang C, Chai J, Shi Y, Xue D. 2002. Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298:1587-1592.
67. Whitmarsh AJ, Davis RJ. 1996. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 74:589-607.
68. Williams GT, Smith CA. 1993. Molecular regulation of apoptosis: Genetic controls on cell death. Cell 74:777-779.
69. Xiong W, Parsons JT. 1997. Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally related to focal adhesion kinase. J Cell Biol 139:529-539.
70. Yamamoto N, Gupta A, Xu M, Miki K, Tsujimoto Y, Tsuchiya H, Tomita K, Moosa AE, Hoffman RM. 2003. Methioninase gene therapy with selenomethionine induces apoptosis in bcl-2-overeproducing lung cancer cells. Cancer Gene Ther 10:445-450.
71. Yoshioka T, Wada T, Uchida N, Maki H, Yoshida H, Ide N, Kasai H, Hojo K, Shono K, Maekawa R, Yagi S, Hoffman RM, Sugita K. 1998. Anticancer efficacy in vivo and in vitro, synergy with 5-fluorouracil, and safety of recombinant methioninase. Cancer Res 58:2583-2587.
72. Yu B, Chang TM. 2004. Polyhemoglobin-tyrosinase, an oxygen carrier with murine B16F10 melanoma suppression properties: A preliminary report. Artif Cells Blood Substit Immobil Biotechnol 32:293-302.
73. Zamzami N, Brenner C, Marzo I, Susin SA, Kroemer G. 1998. Subcellular and submitochondrial mode of action of bcl-2-like oncoproteins. Oncogene 16:2265-2282.
74. Zang M, Hayne C, Luo Z. 2002. Interaction between active Pak1 and Raf-1 is necessary for phosphorylation and activation of Raf-1. J Biol Chem 277:4395-4405.
75. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not Bcl-XL. Cell 87:619-628.
76. Zheng W-H, Kar S, Quirion R. 2000. Stimulation of protein kinase C modulates insulin-like growth factor-1-induced Akt activation in PC12 cells. J Biol Chem 275:13377-13385.
77. Zhou H, Li X-M, Meinkoth J, Pittman RN. 2000. Akt regulates cell survival and apoptosis at a postmitochondrial level. J Cell Biology 151:483-494.
78. Zimmermann S, Moelling K. 1999. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286:1741-1744.