Surviving hypoxia by modulation of mRNA translation rate

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 9 A, 2009, Pages 2770-2779

  Fähling, Michael ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

AMPK; EEF; EIF; Hypoxia; IRES; mRNA translation; MTOR; PERK; PI3K Akt; Post transcriptional control

Indexed keywords

MESSENGER RNA;

ANIMAL; CELL HYPOXIA; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; OXYGEN CONSUMPTION; PROTEIN SYNTHESIS; REVIEW;

ANIMALS; CELL HYPOXIA; CELL SURVIVAL; GENE EXPRESSION REGULATION; HUMANS; OXYGEN CONSUMPTION; PROTEIN BIOSYNTHESIS; RNA, MESSENGER;

EID: 72849129687     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00875.x     Document Type: Review

References (111)

1. Fähling M. Cellular oxygen sensing, signalling and how to survive translational arrest in hypoxia. Acta Physiol. 2009 195 : 205 230.
2. Harris AL. Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer. 2002 2 : 38 47.
3. Lopez-Barneo J, del Toro R, Levitsky KL, et al. Regulation of oxygen sensing by ion channels. J Appl Physiol. 2004 96 : 1187 1195.
4. Vaupel P, Hockel M, Mayer A. Detection and characterization of tumor hypoxia using pO2 histography. Antioxid Redox Signal. 2007 9 : 1221 1235.
5. Giaccia AJ, Simon MC, Johnson R. The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease. Genes Dev. 2004 18 : 2183 2194.
6. Storey KB, Storey JM. Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev Camb Philos Soc. 2004 79 : 207 233.
7. Ebbesen P, Pettersen EO, Gorr TA, et al. Taking advantage of tumor cell adaptations to hypoxia for developing new tumor markers and treatment strategies. J Enzyme Inhib Med Chem. 2009 24 : 1 39.
8. Rolfe DF, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev. 1997 77 : 731 758.
9. Hochachka PW, Buck LT, Doll CJ, et al. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA. 1996 93 : 9493 9498.
10. Chung FZ, Weber HW, Appleman MM. Extensive but reversible depletion of ATP via adenylate cyclase in rat adipocytes. Proc Natl Acad Sci USA. 1985 82 : 1614 1617.
11. Holz MK, Ballif BA, Gygi SP, et al. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell. 2005 123 : 569 580.
12. Scheper GC, van der Knaap MS, Proud CG. Translation matters: protein synthesis defects in inherited disease. Nat Rev Genet. 2007 8 : 711 723.
13. Storey KB, Hochachka PW. Enzymes of energy metabolism from a vertebrate facultative anaerobe, Pseudemys scripta. Turtle heart phosphofructokinase. J Biol Chem. 1974 249 : 1417 1422.
14. Hochachka PW. Defense strategies against hypoxia and hypothermia. Science. 1986 231 : 234 241.
15. Lutz PL. Mechanisms for anoxic survival in the vertebrate brain. Annu Rev Physiol. 1992 54 : 601 618.
16. Storey KB. Metabolic adaptations supporting anoxia tolerance in reptiles: recent advances. Comp Biochem Physiol B Biochem Mol Biol. 1996 113 : 23 35.
17. Hand SC. Oxygen, pHi and arrest of biosynthesis in brine shrimp embryos. Acta Physiol Scand. 1997 161 : 543 551.
18. Ibarguren I, Diaz-Enrich MJ, Cao J, et al. Regulation of the futile cycle of fructose phosphate in sea mussel. Comp Biochem Physiol B Biochem Mol Biol. 2000 126 : 495 501.
19. Boutilier RG. Mechanisms of metabolic defense against hypoxia in hibernating frogs. Respir Physiol. 2001 128 : 365 377.
20. Larade K, Storey KB. Reversible suppression of protein synthesis in concert with polysome disaggregation during anoxia exposure in Littorina littorea. Mol Cell Biochem. 2002 232 : 121 127.
21. Tinton S, Calderon PB. Role of protein phosphorylation in the inhibition of protein synthesis caused by hypoxia in rat hepatocytes. Int J Toxicol. 2001 20 : 21 7.
22. Guppy M, Withers P. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc. 1999 74 : 1 40.
23. Pettersen EO, Juul NO, Ronning OW. Regulation of protein metabolism of human cells during and after acute hypoxia. Cancer Res. 1986 46 : 4346 4351.
24. Storey KB. Mammalian hibernation. Transcriptional and translational controls. Adv Exp Med Biol. 2003 543 : 21 38.
25. DeGracia DJ, Kumar R, Owen CR, et al. Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J Cereb Blood Flow Metab. 2002 22 : 127 141.
26. Anderson LL, Mao X, Scott BA, et al. Survival from hypoxia in C. elegans by inactivation of aminoacyl-tRNA synthetases. Science. 2009 323 : 630 633.
27. Gladden LB. Lactate metabolism: a new paradigm for the third millennium. J Physiol. 2004 558 : 5 30.
28. Kuznetsov AV, Janakiraman M, Margreiter R, et al. Regulating cell survival by controlling cellular energy production: novel functions for ancient signaling pathways FEBS Lett. 2004 577 : 1 4.
29. Mekhail K, Rivero-Lopez L, Khacho M, et al. Restriction of rRNA synthesis by VHL maintains energy equilibrium under hypoxia. Cell Cycle. 2006 5 : 2401 2413.
30. Gebauer F, Hentze MW. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol. 2004 5 : 827 835.
31. Liu L, Cash TP, Jones RG, et al. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell. 2006 21 : 521 531.
32. Thomas JD, Johannes GJ. Identification of mRNAs that continue to associate with polysomes during hypoxia. RNA. 2007 13 : 1116 1131.
33. Koritzinsky M, Magagnin MG, van den Beucken T, et al. Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J. 2006 25 : 1114 1125.
34. Land SC, Hochachka PW. Protein turnover during metabolic arrest in turtle hepatocytes: role and energy dependence of proteolysis. Am J Physiol. 1994 266 : C1028 36.
35. Hand SC. Quiescence in Artemia franciscana embryos: reversible arrest of metabolism and gene expression at low oxygen levels. J Exp Biol. 1998 201 : 1233 1242.
36. Thomas JD, Dias LM, Johannes GJ. Translational repression during chronic hypoxia is dependent on glucose levels. RNA. 2008 14 : 771 781.
37. Fähling M, Steege A, Mrowka R, et al. Rate of protein synthesis under hypometabolic conditions: the down and up and down. FASEB J. 2008 22 : 1174.
38. van den Beucken T, Koritzinsky M, Wouters BG. Translational control of gene expression during hypoxia. Cancer Biol Ther. 2006 5 : 749 755.
39. Ingwall JS. Energy metabolism in heart failure and remodelling. Cardiovasc Res. 2009 81 : 412 419.
40. Iyer NV, Kotch LE, Agani F, et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 1998 12 : 149 162.
41. Clemens MJ, Bommer UA. Translational control: the cancer connection. Int J Biochem Cell Biol. 1999 31 : 1 23.
42. Preiss T, Hentze MW. From factors to mechanisms: translation and translational control in eukaryotes. Curr Opin Genet Dev. 1999 9 : 515 521.
43. Dever TE. Gene-specific regulation by general translation factors. Cell. 2002 108 : 545 556.
44. Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell. 2002 108 : 557 572.
45. Proud CG. Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J. 2007 403 : 217 234.
46. Steitz TA. A structural understanding of the dynamic ribosome machine. Nat Rev Mol Cell Biol. 2008 9 : 242 253.
47. Zaher HS, Green R. Fidelity at the molecular level: lessons from protein synthesis. Cell. 2009 136 : 746 762.
48. Kozak M. Initiation of translation in prokaryotes and eukaryotes. Gene. 1999 234 : 187 208.
49. Sonenberg N, Hinnebusch AG. New modes of translational control in development, behavior, and disease. Mol Cell. 2007 28 : 721 729.
50. Preiss T, Hentze W. Starting the protein synthesis machine: eukaryotic translation initiation. Bioessays. 2003 25 : 1201 1211.
51. Blais JD, Filipenko V, Bi M, et al. Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol Cell Biol. 2004 24 : 7469 7482.
52. Kimball SR. Eukaryotic initiation factor eIF2. Int J Biochem Cell Biol. 1999 31 : 25 9.
53. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. 1999 397 : 271 274.
54. Koumenis C, Wouters BG. "Translating" tumor hypoxia: unfolded protein response (UPR)-dependent and UPR-independent pathways. Mol Cancer Res. 2006 4 : 423 436.
55. Koumenis C, Naczki C, Koritzinsky M, et al. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol. 2002 22 : 7405 7416.
56. Gingras AC, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 2001 15 : 807 826.
57. Ma XM, Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol. 2009 10 : 307 318.
58. Arsham AM, Howell JJ, Simon MC. A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J Biol Chem. 2003 278 : 29655 29660.
59. Brugarolas J, Lei K, Hurley RL, et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 2004 18 : 2893 2904.
60. Dubois L, Magagnin MG, Cleven AH, et al. Inhibition of 4E-BP1 sensitizes U87 glioblastoma xenograft tumors to irradiation by decreasing hypoxia tolerance. Int J Radiat Oncol Biol Phys. 2009 73 : 1219 1227.
61. Magagnin MG, van den Beucken T, Sergeant K, et al. The mTOR target 4E-BP1 contributes to differential protein expression during normoxia and hypoxia through changes in mRNA translation efficiency. Proteomics. 2008 8 : 1019 1028.
62. Wang X, Li W, Williams M, et al. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J. 2001 20 : 4370 4379.
63. Reiling JH, Sabatini DM. Stress and mTORture signaling. Oncogene. 2006 25 : 6373 6383.
64. Wouters BG, Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer. 2008 8 : 851 864.
65. Inoki K, Li Y, Xu T, Guan KL. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 2003 17 : 1829 1834.
66. Borger DR, Gavrilescu LC, Bucur MC, et al. AMP-activated protein kinase is essential for survival in chronic hypoxia. Biochem Biophys Res Commun. 2008 370 : 230 234.
67. Gwinn DM, Shackelford DB, Egan DF, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008 30 : 214 226.
68. Horman S, Browne G, Krause U, et al. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol. 2002 12 : 1419 1423.
69. Chen G, Gharib TG, Huang CC, et al. Discordant protein and mRNA expression in lung adenocarcinomas. Mol Cell Proteomics. 2002 1 : 304 313.
70. Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol. 1999 19 : 1720 1730.
71. Fähling M, Steege A, Perlewitz A, et al. Role of nucleolin in posttranscriptional control of MMP-9 expression. Biochim Biophys Acta. 2005 1731 : 32 40.
72. Fähling M, Mrowka R, Steege A, et al. Translational control of collagen prolyl 4-hydroxylase-alpha(I) gene expression under hypoxia. J Biol Chem. 2006 281 : 26089 26101.
73. Fähling M, Mrowka R, Steege A, et al. Translational regulation of the human achaete-scute homologue-1 by fragile X mental retardation protein. J Biol Chem. 2009 284 : 4255 4266.
74. Ufer C, Wang CC, Fähling M, et al. Translational regulation of glutathione peroxidase 4 expression through guanine-rich sequence-binding factor 1 is essential for embryonic brain development. Genes Dev. 2008 22 : 1838 1850.
75. Koritzinsky M, Seigneuric R, Magagnin MG, et al. The hypoxic proteome is influenced by gene-specific changes in mRNA translation. Radiother Oncol. 2005 76 : 177 186.
76. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004 116 : 281 297.
77. Dalmay T, Edwards DR. MicroRNAs and the hallmarks of cancer. Oncogene. 2006 25 : 6170 6175.
78. Chu CY, Rana TM. Small RNAs: regulators and guardians of the genome. J Cell Physiol. 2007 213 : 412 419.
79. Meister G. miRNAs get an early start on translational silencing. Cell. 2007 131 : 25 8.
80. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight Nat Rev Genet. 2008 9 : 102 114.
81. Czyzyk-Krzeska MF, Beresh JE. Characterization of the hypoxia-inducible protein binding site within the pyrimidine-rich tract in the 3′-untranslated region of the tyrosine hydroxylase mRNA. J Biol Chem. 1996 271 : 3293 3299.
82. Donker RB, Mouillet JF, Nelson DM, Sadovsky Y. The expression of Argonaute2 and related microRNA biogenesis proteins in normal and hypoxic trophoblasts. Mol Hum Reprod. 2007 13 : 273 279.
83. Kulshreshtha R, Ferracin M, Negrini M, et al. Regulation of microRNA expression: the hypoxic component. Cell Cycle. 2007 6 : 1426 1431.
84. Fasanaro P, D'Alessandra Y, Di S, et al. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem. 2008 283 : 15878 15883.
85. Giannakakis A, Sandaltzopoulos R, Greshock J, et al. miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer. Cancer Biol Ther. 2008 7 : 255 264.
86. Kulshreshtha R, Ferracin M, Wojcik SE, et al. A microRNA signature of hypoxia. Mol Cell Biol. 2007 27 : 1859 1867.
87. Oh N, Kim KM, Choe J, Kim YK. Pioneer round of translation mediated by nuclear cap-binding proteins CBP80/20 occurs during prolonged hypoxia. FEBS Lett. 2007 581 : 5158 5164.
88. Levine T, Rabouille C. Endoplasmic reticulum: one continuous network compartmentalized by extrinsic cues. Curr Opin Cell Biol. 2005 17 : 362 368.
89. Christensen AK, Kahn LE, Bourne CM. Circular polysomes predominate on the rough endoplasmic reticulum of somatotropes and mammotropes in the rat anterior pituitary. Am J Anat. 1987 178 : 1 10.
90. Lerner RS, Nicchitta CV. mRNA translation is compartmentalized to the endoplasmic reticulum following physiological inhibition of cap-dependent translation. RNA. 2006 12 : 775 789.
91. Stephens SB, Dodd RD, Brewer JW, et al. Stable ribosome binding to the endoplasmic reticulum enables compartment-specific regulation of mRNA translation. Mol Biol Cell. 2005 16 : 5819 5831.
92. Anderson P, Kedersha N. RNA granules. J Cell Biol. 2006 172 : 803 808.
93. Anderson P, Kedersha N. Stressful initiations. J Cell Sci. 2002 115 : 3227 3234.
94. Kedersha NL, Gupta M, Li W, et al. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol. 1999 147 : 1431 1442.
95. McEwen E, Kedersha N, Song B, et al. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem. 2005 280 : 16925 16933.
96. Lopez-Lastra M, Rivas A, Barria MI. Protein synthesis in eukaryotes: the growing biological relevance of cap-independent translation initiation. Biol Res. 2005 38 : 121 146.
97. Graber TE, Holcik M. Cap-independent regulation of gene expression in apoptosis. Mol Biosyst. 2007 3 : 825 834.
98. Nakamoto T. The initiation of eukaryotic and prokaryotic protein synthesis: a selective accessibility and multisubstrate enzyme reaction. Gene. 2007 403 : 1 5.
99. Nakamoto T. Evolution and the universality of the mechanism of initiation of protein synthesis. Gene. 2009 432 : 1 6.
100. Shirokikh NE, Spirin AS. Poly(A) leader of eukaryotic mRNA bypasses the dependence of translation on initiation factors. Proc Natl Acad Sci USA. 2008 105 : 10738 10743.
101. Pende M, Um SH, Mieulet V, et al. S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol. 2004 24 : 3112 3124.
102. Jastrzebski K, Hannan KM, Tchoubrieva EB, et al. Coordinate regulation of ribosome biogenesis and function by the ribosomal protein S6 kinase, a key mediator of mTOR function. Growth Factors. 2007 25 : 209 226.
103. Brown JM, Wilson WR. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer. 2004 4 : 437 447.
104. Montanaro L, Trere D, Derenzini M. Nucleolus, ribosomes, and cancer. Am J Pathol. 2008 173 : 301 310.
105. Ruggero D, Pandolfi PP. Does the ribosome translate cancer Nat Rev Cancer. 2003 3 : 179 192.
106. Lee JW, Beebe K, Nangle LA, et al. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature. 2006 443 : 50 55.
107. Nagatomo Y, Carabello BA, Hamawaki M, et al. Translational mechanisms accelerate the rate of protein synthesis during canine pressure-overload hypertrophy. Am J Physiol. 1999 277 : H2176 84.
108. Hannan RD, Jenkins A, Jenkins AK, et al. Cardiac hypertrophy: a matter of translation. Clin Exp Pharmacol Physiol. 2003 30 : 517 527.
109. Kasinath BS, Mariappan MM, Sataranatarajan K, et al. Novel mechanisms of protein synthesis in diabetic nephropathy-role of mRNA translation. Rev Endocr Metab Disord. 2008 9 : 255 266.
110. Komili S, Farny NG, Roth FP, et al. Functional specificity among ribosomal proteins regulates gene expression. Cell. 2007 131 : 557 571.
111. Mauro VP, Edelman GM. The ribosome filter hypothesis. Proc Natl Acad Sci USA. 2002 99 : 12031 12036.