Acidosis promotes Bcl-2 family-mediated evasion of apoptosis: Involvement of acid-sensing G protein-coupled receptor GPR65 signaling to MEK/ERK

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27863-27875

  Ryder, Christopher ^a   McColls, Karen ^a   Zhongs, Fei ^a   Distelhorst, Clark W ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC CONDITIONS; APOPTOSIS REGULATOR; BCL-2 AND BCL-XL; BCL-2 FAMILY; CYTOTOXIC; DEXAMETHASONES; G PROTEIN COUPLED RECEPTORS; LYMPHOID MALIGNANCIES; LYMPHOMA CELLS; METABOLIC STRESS; NUTRIENT SUPPLY;

AMINO ACIDS; ANIMAL CELL CULTURE; BIOELECTRIC POTENTIALS; GLUCOSE;

CELL DEATH;

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BIM PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DEXAMETHASONE; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 65; GLUCOSE; GLUTAMINE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 2; PROTEIN BCL XL; PUMA PROTEIN; UNCLASSIFIED DRUG;

ACIDOSIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PH; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOMA CELL; METABOLIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; UPREGULATION;

ACIDOSIS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-X PROTEIN; BIPHENYL COMPOUNDS; HUMANS; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICE; NITROPHENOLS; PIPERAZINES; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SULFONAMIDES; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84864974250     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.384685     Document Type: Article

References (75)

1. Evelhoch, J. L. (2001) pH and therapy of human cancers. Novartis Found. Symp. 240, 68-80; discussion 80-4, 152-3
2. Vaupel, P., Kallinowski, F., and Okunieff, P. (1989) Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 49, 6449-6465
3. Mortensen, B. T., Jensen, P. O., Helledie, N., Iversen, P. O., Ralfkiaer, E., Larsen, J. K., and Madsen, M. T. (1998) Changing bone marrow microenvironment during development of acute myeloid leukaemia in rats. Br. J. Haematol. 102, 458-464
4. Parks, S. K., Chiche, J., and Pouyssegur, J. (2011) pH control mechanisms of tumor survival and growth. J. Cell. Physiol. 226, 299-308
5. Reichert, M., Steinbach, J. P., Supra, P., and Weller, M. (2002) Modulation of growth and radiochemosensitivity of human malignant glioma cells by acidosis. Cancer 95, 1113-1119
6. Thews, O., Gassner, B., Kelleher, D. K., Schwerdt, G., and Gekle, M. (2007) Impact of hypoxic and acidic extracellular conditions on cytotoxicity of chemotherapeutic drugs. Adv. Exp. Med. Biol. 599, 155-161
7. McCarty, M. F., and Whitaker, J. (2010) Manipulating tumor acidification as a cancer treatment strategy. Altern. Med. Rev. 15, 264-272
8. De Milito, A., and Fais, S. (2005) Tumor acidity, chemoresistance and proton pump inhibitors. Future Oncol. 1, 779-786
9. Moyer, G. H., and Pitot, H. C. (1974) Static and dynamic aspects of amino acid pools in rat liver and Morris hepatomas 9618A and 7800. Cancer Res. 34, 2647-2653
10. DeBerardinis, R. J., and Cheng, T. (2010) Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 29, 313-324
11. Schroeder, T., Yuan, H., Viglianti, B. L., Peltz, C., Asopa, S., Vujaskovic, Z., and Dewhirst, M. W. (2005) Spatial heterogeneity and oxygen dependence of glucose consumption in R3230Ac and fibrosarcomas of the Fischer 344 rat. Cancer Res. 65, 5163-5171
12. Sauer, L. A., Stayman, J. W., 3rd, and Dauchy, R. T. (1982) Amino acid, glucose, and lactic acid utilization in vivo by rat tumors. Cancer Res. 42, 4090-4097
13. Eagle, H. (1955) Nutrition needs of mammalian cells in tissue culture. Science 122, 501-514
14. Fuchs, B. C., and Bode, B. P. (2006) Stressing out over survival: glutamine as an apoptotic modulator. J. Surg. Res. 131, 26-40
15. Yuneva, M., Zamboni, N., Oefner, P., Sachidanandam, R., and Lazebnik, Y. (2007) Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J. Cell Biol. 178, 93-105
16. El Mjiyad, N., Caro-Maldonado, A., Ramírez-Peinado, S., and Muñoz-Pinedo, C. (2011) Sugar-free approaches to cancer cell killing. Oncogene 30, 253-264
17. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70
18. Tsujimoto, Y., Finger, L. R., Yunis, J., Nowell, P. C., and Croce, C. M. (1984) Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226, 1097-1099
19. Hockenbery, D. M. (2010) Targeting mitochondria for cancer therapy. Environ. Mol. Mutagen. 51, 476-489
20. Chipuk, J. E., Moldoveanu, T., Llambi, F., Parsons, M. J., and Green, D. R. (2010) The BCL-2 family reunion. Mol. Cell 37, 299-310
21. Letai, A. (2005) Pharmacological manipulation of Bcl-2 family members to control cell death. J. Clin. Invest. 115, 2648-2655
22. Wang, J. Q., Kon, J., Mogi, C., Tobo, M., Damirin, A., Sato, K., Komachi, M., Malchinkhuu, E., Murata, N., Kimura, T., Kuwabara, A., Wakamatsu, K., Koizumi, H., Uede, T., Tsujimoto, G., Kurose, H., Sato, T., Harada, A., Misawa, N., Tomura, H., and Okajima, F. (2004) TDAG8 is a proton-sensing and psychosine-sensitive G-protein-coupled receptor. J. Biol. Chem. 279, 45626-45633
23. Ishii, S., Kihara, Y., and Shimizu, T. (2005) Identification of T cell death-associated gene 8 (TDAG8) as a novel acid sensing G-protein-coupled receptor. J. Biol. Chem. 280, 9083-9087
24. Sin, W. C., Zhang, Y., Zhong, W., Adhikarakunnathu, S., Powers, S., Hoey, T., An, S., and Yang, J. (2004) G protein-coupled receptors GPR4 and TDAG8 are oncogenic and overexpressed in human cancers. Oncogene 23, 6299-6303
25. Ihara, Y., Kihara, Y., Hamano, F., Yanagida, K., Morishita, Y., Kunita, A., Yamori, T., Fukayama, M., Aburatani, H., Shimizu, T., and Ishii, S. (2010) The G protein-coupled receptor T-cell death-associated gene 8 (TDAG8) facilitates tumor development by serving as an extracellular pH sensor. Proc. Natl. Acad. Sci. U.S.A. 107, 17309-17314
26. Li, S., Huang, S., and Peng, S. B. (2005) Overexpression of G protein-coupled receptors in cancer cells: involvement in tumor progression. Int. J. Oncol. 27, 1329-1339
27. Kottyan, L. C., Collier, A. R., Cao, K. H., Niese, K. A., Hedgebeth, M., Radu, C. G., Witte, O. N., Khurana Hershey, G. K., Rothenberg, M. E., and Zimmermann, N. (2009) Eosinophil viability is increased by acidic pH in a cAMP- and GPR65-dependent manner. Blood 114, 2774-2782
28. McGuire, J., Herman, J. P., Ghosal, S., Eaton, K., Sallee, F. R., and Sah, R. (2009) Acid-sensing by the T cell death-associated gene 8 (TDAG8) receptor cloned from rat brain. Biochem. Biophys. Res. Commun. 386, 420-425
29. Chen, R., Valencia, I., Zhong, F., McColl, K. S., Roderick, H. L., Bootman, M. D., Berridge, M. J., Conway, S. J., Holmes, A. B., Mignery, G. A., Velez, P., and Distelhorst, C. W. (2004) Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1,4,5-trisphosphate. J. Cell Biol. 166, 193-203
30. Radu, C. G., Nijagal, A., McLaughlin, J., Wang, L., and Witte, O. N. (2005) Differential proton sensitivity of related G protein-coupled receptors T cell death-associated gene 8 and G2A expressed in immune cells. Proc. Natl. Acad. Sci. U.S.A. 102, 1632-1637
31. Thews, O., Gassner, B., Kelleher, D. K., Schwerdt, G., and Gekle, M. (2006) Impact of extracellular acidity on the activity of P-glycoprotein and the cytotoxicity of chemotherapeutic drugs. Neoplasia 8, 143-152
32. Dowd, D. R., and Miesfeld, R. L. (1992) Evidence that glucocorticoid- and cyclic AMP-induced apoptotic pathways in lymphocytes share distal events. Mol. Cell. Biol. 12, 3600-3608
33. Molitoris, J. K., McColl, K. S., and Distelhorst, C. W. (2011) Glucocorticoid-mediated repression of the oncogenic microRNA cluster miR-17-92 contributes to the induction of Bim and initiation of apoptosis. Mol. Endocrinol. 25, 409-420
34. Rosen, J. M., Milholland, R. J., and Rosen, F. (1970) A comparison of the effect of glucocorticoids on glucose uptake and hexokinase activity in lymphosarcoma P1798. Biochim. Biophys. Acta 219, 447-454
35. Wise, D. R., and Thompson, C. B. (2010) Glutamine addiction: a new therapeutic target in cancer. Trends Biochem. Sci. 35, 427-433
36. Dang, C. V. (2010) Rethinking the Warburg effect with Myc micromanaging glutamine metabolism. Cancer Res. 70, 859-862
37. Marrack, P., and Kappler, J. (2004) Control of T cell viability. Annu. Rev. Immunol. 22, 765-787
38. Chang, W. K., Yang, K. D., Chuang, H., Jan, J. T., and Shaio, M. F. (2002) Glutamine protects activated human T cells from apoptosis by up-regulating glutathione and Bcl-2 levels. Clin. Immunol. 104, 151-160
39. Coloff, J. L., Mason, E. F., Altman, B. J., Gerriets, V. A., Liu, T., Nichols, A. N., Zhao, Y., Wofford, J. A., Jacobs, S. R., Ilkayeva, O., Garrison, S. P., Zambetti, G. P., and Rathmell, J. C. (2011) Akt requires glucose metabolism to suppress PUMA expression and prevent apoptosis of leukemic T cells. J. Biol. Chem. 286, 5921-5933
40. Certo, M., Del Gaizo Moore, V., Nishino, M., Wei, G., Korsmeyer, S., Armstrong, S. A., and Letai, A. (2006) Mitochondria primed by death signals determine cellular addiction to antiapoptotic Bcl-2 family members. Cancer Cell 9, 351-365
41. Petros, A. M., Dinges, J., Augeri, D. J., Baumeister, S. A., Betebenner, D. A., Bures, M. G., Elmore, S. W., Hajduk, P. J., Joseph, M. K., Landis, S. K., Nettesheim, D. G., Rosenberg, S. H., Shen, W., Thomas, S., Wang, X., Zanze, I., Zhang, H., and Fesik, S. W. (2006) Discovery of a potent inhibitor of the antiapoptotic protein Bcl-xL from NMR and parallel synthesis. J. Med. Chem. 49, 656-663
42. Vogler, M., Dinsdale, D., Dyer, M. J., and Cohen, G. M. (2009) Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ. 16, 360-367
43. Malone, M. H., Wang, Z., and Distelhorst, C. W. (2004) The glucocorticoid-induced gene tdag8 encodes a pro-apoptotic G protein-coupled receptor whose activation promotes glucocorticoid-induced apoptosis. J. Biol. Chem. 279, 52850-52859
44. Wilson, B. E., Mochon, E., and Boxer, L. M. (1996) Induction of Bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol. Cell. Biol. 16, 5546-5556
45. Murray, A. J. (2008) Pharmacological PKA inhibition: all may not be what it seems. Sci. Signal 1, re4
46. Pearson, G., Robinson, F., Beers Gibson, T., Xu, B. E., Karandikar, M., Berman, K., and Cobb, M. H. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153-183
47. Liu, Y. Z., Boxer, L. M., and Latchman, D. S. (1999) Activation of the Bcl-2 promoter by nerve growth factor is mediated by the p42/p44 MAPK cascade. Nucleic Acids Res. 27, 2086-2090
48. Squires, M. S., Nixon, P. M., and Cook, S. J. (2002) Cell-cycle arrest by PD184352 requires inhibition of extracellular signal-regulated kinases (ERK) 1/2 but not ERK5/BMK1. Biochem. J. 366, 673-680
49. Meads, M. B., Hazlehurst, L. A., and Dalton, W. S. (2008) The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin. Cancer Res. 14, 2519-2526
50. Gatenby, R. A., and Gillies, R. J. (2004) Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 4, 891-899
51. Kubasiak, L. A., Hernandez, O. M., Bishopric, N. H., and Webster, K. A. (2002) Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc. Natl. Acad. Sci. U.S.A. 99, 12825-12830
52. Jeong, D., Kim, T. S., Lee, J. W., Kim, K. T., Kim, H. J., Kim, I. H., and Kim, I. Y. (2001) Blocking of acidosis-mediated apoptosis by a reduction of lactate dehydrogenase activity through antisense mRNA expression. Biochem. Biophys. Res. Commun. 289, 1141-1149
53. Ding, D., Moskowitz, S. I., Li, R., Lee, S. B., Esteban, M., Tomaselli, K., Chan, J., and Bergold, P. J. (2000) Acidosis induces necrosis and apoptosis of cultured hippocampal neurons. Exp. Neurol. 162, 1-12
54. Raghunand, N., He, X., van Sluis, R., Mahoney, B., Baggett, B., Taylor, C. W., Paine-Murrieta, G., Roe, D., Bhujwalla, Z. M., and Gillies, R. J. (1999) Enhancement of chemotherapy by manipulation of tumour pH. Br. J. Cancer 80, 1005-1011
55. Jazirehi, A. R., Vega, M. I., Chatterjee, D., Goodglick, L., and Bonavida, B. (2004) Inhibition of the Raf-MEK1/2-ERK1/2 signaling pathway, Bcl-xL down-regulation, and chemosensitization of non-Hodgkin's lymphoma B cells by rituximab. Cancer Res. 64, 7117-7126
56. Pardo, O. E., Arcaro, A., Salerno, G., Raguz, S., Downward, J., and Seckl, M. J. (2002) Fibroblast growth factor-2 induces translational regulation of Bcl-xL and Bcl-2 via a MEK-dependent pathway: correlation with resistance to etoposide-induced apoptosis. J. Biol. Chem. 277, 12040-12046
57. Flacke, J. P., Kumar, S., Kostin, S., Reusch, H. P., and Ladilov, Y. (2009) Acidic preconditioning protects endothelial cells against apoptosis through p38- and Akt-dependent Bcl-xL overexpression. Apoptosis 14, 90-96
58. Willimott, S., and Wagner, S. D. (2010) Post-transcriptional and post-translational regulation of Bcl2. Biochem. Soc. Trans. 38, 1571-1575
59. Holcik, M., Yeh, C., Korneluk, R. G., and Chow, T. (2000) Translational up-regulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death. Oncogene 19, 4174-4177
60. Reed, J. C., Tsujimoto, Y., Epstein, S. F., Cuddy, M., Slabiak, T., Nowell, P. C., and Croce, C. M. (1989) Regulation of Bcl-2 gene expression in lymphoid cell lines containing normal #18 or t(14;18) chromosomes. Oncogene Res. 4, 271-282
61. Ishimaru, D., Zuraw, L., Ramalingam, S., Sengupta, T. K., Bandyopadhyay, S., Reuben, A., Fernandes, D. J., and Spicer, E. K. (2010) Mechanism of regulation of Bcl-2 mRNA by nucleolin and A+U-rich element-binding factor 1 (AUF1). J. Biol. Chem. 285, 27182-27191
62. Lapucci, A., Lulli, M., Amedei, A., Papucci, L., Witort, E., Di Gesualdo, F., Bertolini, F., Brewer, G., Nicolin, A., Bevilacqua, A., Schiavone, N., Morello, D., Donnini, M., and Capaccioli, S. (2010) ζ-Crystallin is a bcl-2 mRNA binding protein involved in Bcl-2 overexpression in T-cell acute lymphocytic leukemia. FASEB J. 24, 1852-1865
63. Sengupta, T. K., Bandyopadhyay, S., Fernandes, D. J., and Spicer, E. K. (2004) Identification of nucleolin as an AU-rich element binding protein involved in Bcl-2 mRNA stabilization. J. Biol. Chem. 279, 10855-10863
64. Wensveen, F. M., Alves, N. L., Derks, I. A., Reedquist, K. A., and Eldering, E. (2011) Apoptosis induced by overall metabolic stress converges on the Bcl-2 family proteins Noxa and Mcl-1. Apoptosis 16, 708-721
65. Balmanno, K., and Cook, S. J. (2009) Tumour cell survival signalling by the ERK1/2 pathway. Cell Death Differ. 16, 368-377
66. Fricker, M., O'Prey, J., Tolkovsky, A. M., and Ryan, K. M. (2010) Phosphorylation of PUMA modulates its apoptotic function by regulating protein stability. Cell Death Dis. 1, e59
67. Yu, J., and Zhang, L. (2008) PUMA, a potent killer with or without p53. Oncogene 27, Suppl, 1, S71-83
68. Zhang, W., Konopleva, M., Burks, J. K., Dywer, K. C., Schober, W. D., Yang, J. Y., McQueen, T. J., Hung, M. C., and Andreeff, M. (2010) Blockade of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase and murine double minute synergistically induces apoptosis in acute myeloid leukemia via BH3-only proteins PUMA and Bim. Cancer Res. 70, 2424-2434
69. Wang, Y. F., Jiang, C. C., Kiejda, K. A., Gillespie, S., Zhang, X. D., and Hersey, P. (2007) Apoptosis induction in human melanoma cells by inhibition of MEK is caspase-independent and mediated by the Bcl-2 family members PUMA, Bim, and Mcl-1. Clin. Cancer Res. 13, 4934-4942
70. Gerits, N., Kostenko, S., Shiryaev, A., Johannessen, M., and Moens, U. (2008) Relations between the mitogen-activated protein kinase and the cAMP-dependent protein kinase pathways: comradeship and hostility. Cell. Signal. 20, 1592-1607
71. Shi, Y., Feng, Y., Kang, J., Liu, C., Li, Z., Li, D., Cao, W., Qiu, J., Guo, Z., Bi, E., Zang, L., Lu, C., Zhang, J. Z., and Pei, G. (2007) Critical regulation of CD4+ T cell survival and autoimmunity by β-arrestin 1. Nat. Immunol. 8, 817-824
72. Laroche-Joubert, N., Marsy, S., Michelet, S., Imbert-Teboul, M., and Doucet, A. (2002) Protein kinase A-independent activation of ERK and H,K-ATPase by cAMP in native kidney cells: role of Epac I. J. Biol. Chem. 277, 18598-18604
73. Chen, A., Dong, L., Leffler, N. R., Asch, A. S., Witte, O. N., and Yang, L. V. (2011) Activation of GPR4 by acidosis increases endothelial cell adhesion through the cAMP/Epac pathway. PLoS One 6, e27586
74. Radu, C. G., Cheng, D., Nijagal, A., Riedinger, M., McLaughlin, J., Yang, L. V., Johnson, J., and Witte, O. N. (2006) Normal immune development and glucocorticoid-induced thymocyte apoptosis in mice deficient for the T-cell death-associated gene 8 receptor. Mol. Cell. Biol. 26, 668-677
75. Klymenko, T., Brandenburg, M., Morrow, C., Dive, C., and Makin, G. (2011) The novel Bcl-2 inhibitor ABT-737 is more effective in hypoxia and is able to reverse hypoxia-induced drug resistance in neuroblastoma cells. Mol. Cancer Ther. 10, 2373-2383