Aglycemia keeps mitochondrial oxidative phosphorylation under hypoxic conditions in HepG2 cells

Journal of Bioenergetics and Biomembranes

Volumn 47, Issue 6, 2015, Pages 467-476

  Plecitá Hlavatá, Lydie ^a   Ježek, Jan ^a   Ježek, Petr ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

Cancer mitochondria; Glutaminolysis; HepG2 cells; Hypoxia inducible factor; Non canonical response to hypoxia

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; PYRUVATE DEHYDROGENASE;

AEROBIC GLYCOLYSIS; AEROBIC METABOLISM; AGLYCEMIA; APOPTOSIS; ARTICLE; BIOENERGY; CANCER CELL; CELL DEATH; CELL PROLIFERATION; GLUCOSE BLOOD LEVEL; HEPG2 CELL LINE; HUMAN; HUMAN CELL; HYPOXIC CELL; LIVER CELL CARCINOMA; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; RESPIROMETRY; CELL CULTURE TECHNIQUE; CELL HYPOXIA; METABOLISM;

CELL CULTURE TECHNIQUES; CELL HYPOXIA; HEP G2 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION;

EID: 84948070059     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-015-9628-6     Document Type: Article

References (65)

1. Ameri K, Rajah AM, Nguyen V, Sanders TA, Jahangiri A, Delay M, Donne M, Choi HJ, Tormos KV, Yeghiazarians Y, Jeffrey SS, Rinaudo PF, Rowitch DH, Aghi M, Maltepe E (2013) Nuclear localization of the mitochondrial factor HIGD1A during metabolic stress. PLoS One 8:e62758
2. Ameri K, Jahangiri A, Rajah AM, Tormos KV, Nagarajan R, Pekmezci M, Nguyen V, Wheeler ML, Murphy MP, Sanders TA, Jeffrey SS, Yeghiazarians Y, Rinaudo PF, Costello JF, Aghi MK, Maltepe E (2015) HIGD1A regulates oxygen consumption, ROS production, and AMPK activity during glucose deprivation to modulate cell survival and tumor growth. Cell Rep pii:S2211–1247(15)00033–00039.
3. Anderson KA, Hirschey MD (2012) Mitochondrial protein acetylation regulates metabolism. Essays Biochem 52:23–35
4. Baracca A, Sgarbi G, Padula A, Solaini G (2013) Glucose plays a main role in human fibroblasts adaptation to hypoxia. Int J Biochem Cell Biol 45:1356–1365
5. Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GR, Chandel NS (2007) The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 177:1029–1036
6. Bell EL, Emerling BM, Ricoult SJ, Guarente L (2011) SirT3 suppresses hypoxia inducible factor 1α and tumor growth by inhibiting mitochondrial ROS production. Oncogene 30:2986–2996
7. Brocato J, Chervona Y, Costa M (2014) Molecular responses to hypoxia-inducible factor 1α and beyond. Mol Pharmacol 85:651–657
8. Buccellato LJ, Tso M, Akinci OI, Chandel NS, Budinger GR (2004) Reactive oxygen species are required for hyperoxia-induced Bax activation and cell death in alveolar epithelial cells. J Biol Chem 279:6753–6760
9. Cerniglia GJ, Dey S, Gallagher-Colombo SM, Daurio NA, Tuttle S, Busch TM, Lin A, Sun R, Esipova TV, Vinogradov SA, Denko N, Koumenis C, Maity A (2015) The PI3K/Akt pathway regulates oxygen metabolism via pyruvate dehydrogenase (PDH)-E1α phosphorylation. Mol Cancer Ther pii: molcanther.0888.
10. Chandel NS (2010) Mitochondrial complex III: an essential component of universal oxygen sensing machinery? Respir Physiol Neurobiol 174:175–181
11. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 95:11715–11720
12. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834–840
13. Christofk HR, Vander Heiden MG, Wu N, Asara JM, Cantley LC (2008a) Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 452:181–186
14. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, Cantley LC (2008b) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452:230–233
15. Csibi A, Fendt SM, Li C, Poulogiannis G, Choo AY, Chapski DJ, Jeong SM, Dempsey JM, Parkhitko A, Morrison T, Henske EP, Haigis MC, Cantley LC, Stephanopoulos G, Yu J, Blenis J (2013) The mTORC1 pathway stimulates glutamine metabolism and cell proliferation by repressing SIRT4. Cell 153:840–854
16. Denko NC (2008) Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 8:705–713
17. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, Semenza GL (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129:111–122
18. Greer SN, Metcalf JL, Wang Y, Ohh M (2012) The updated biology of hypoxia-inducible factor. Embo J 31:2448–2460
19. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1:401–414
20. Hayashi T, Asano Y, Shintani Y, Aoyama H, Kioka H, Tsukamoto O, Hikita M, Shinzawa-Itoh K, Takafuji K, Higo S, Kato H, Yamazaki S, Matsuoka K, Nakano A, Asanuma H, Asakura M, Minamino T, Goto Y, Ogura T, Kitakaze M, Komuro I, Sakata Y, Tsukihara T, Yoshikawa S, Takashima S (2015) Higd1a is a positive regulator of cytochrome c oxidase. Proc Natl Acad Sci U S A 112:1553–1558
21. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K, Dong S, Lonial S, Wang X, Chen GZ, Xie J, Gu TL, Polakiewicz RD, Roesel JL, Boggon TJ, Khuri FR, Gilliland DG, Cantley LC, Kaufman J, Chen J (2009) Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2:ra73.
22. Hitosugi T, Fan J, Chung TW, Lythgoe K, Wang X, Xie J, Ge Q, Gu TL, Polakiewicz RD, Roesel JL, Chen GZ, Boggon TJ, Lonial S, Fu H, Khuri FR, Kang S, Chen J (2011) Tyrosine phosphorylation of mitochondrial pyruvate dehydrogenase kinase 1 is important for cancer metabolism. Mol Cell 44:864–877
23. Hsu CC, Wang CH, Wu LC, Hsia CY, Chi CW, Yin PH, Chang CJ, Sung MT, Wei YH, Lu SH, Lee HC (2013) Mitochondrial dysfunction represses HIF-1α protein synthesis through AMPK activation in human hepatoma HepG2 cells. Biochim Biophys Acta 1830:4743–4751
24. Hubbi ME, Hu H, Kshitiz NF, Gilkes DM, Semenza GL (2013) Sirtuin-7 inhibits the activity of hypoxia-inducible factors. J Biol Chem 288:20768–20775
25. Ježek P, Plecitá–Hlavatá L, Smolková K, Rossignol R (2010) Distinctions and similarities of cell bioenergetics and role of mitochondria in hypoxia, cancer, and embryonic development. Int J Biochem Cell Biol 42:604–622
26. 2 tension. Am J Physiol Cell Physiol 271:C1172–C1180
27. Jose C, Rossignol R (2013) Rationale for mitochondria-targeting strategies in cancer bioenergetic therapies. Int J Biochem Cell Biol 45:123–129
28. Kai S, Tanaka T, Daijo H, Harada H, Kishimoto S, Suzuki K, Takabuchi S, Takenaga K, Fukuda K, Hirota K (2012) Hydrogen sulfide inhibits hypoxia- but not anoxia-induced hypoxia-inducible factor 1 activation in a von hippel-lindau- and mitochondria-dependent manner. Antioxid Redox Signal 16:203–216
29. Kikuchi D, Minamishima YA, Nakayama K (2014) Prolyl-hydroxylase PHD3 interacts with pyruvate dehydrogenase (PDH)-E1β and regulates the cellular PDH activity. Biochem Biophys Res Commun 451:288–294
30. Kim JW, Tchernyshyov I, Semenza GL, Dang CV (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3:177–185
31. Krall AS, Christofk HR (2013) Cancer: a metabolic metamorphosis. Nature 496:38–40
32. Mansfield KD, Guzy RD, Pan Y, Young RM, Cash TP, Schumacker PT, Simon MC (2005) Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 1:393–399
33. Metallo CM, Gameiro PA, Bell EL, Mattaini KR, Yang J, Hiller K, Jewell CM, Johnson ZR, Irvine DJ, Guarente L, Kelleher JK, Van der Heiden MG, Iliopoulos O, Stephanopoulos G (2011) Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 481:380–384
34. Métrailler-Ruchonnet I, Pagano A, Carnesecchi S, Ody C, Donati Y, Barazzone-Argiroffo C (2007) Bcl-2 protects against hyperoxia-induced apoptosis through inhibition of the mitochondria-dependent pathway. Free Radic Biol Med 42:1062–1074
35. Morava E (2014) Galactose supplementation in phosphoglucomutase-1 deficiency; review and outlook for a novel treatable CDG. Mol Genet Metab 112:275–279
36. Morten KJ, Badder L, Knowles HJ (2013) Differential regulation of HIF-mediated pathways increases mitochondrial metabolism and ATP production in hypoxic osteoclasts. J Pathol 229:755–764
37. Nguyen LK, Cavadas MA, Scholz CC, Fitzpatrick SF, Bruning U, Cummins EP, Tambuwala MM, Manresa MC, Kholodenko BN, Taylor CT, Cheong A (2013) A dynamic model of the hypoxia-inducible factor 1α (HIF-1α) network. J Cell Sci 126:1454–1463
38. 2 generated by NOX4 during cellular response under glucose deprivation. PLoS One 8:e56628
39. Peserico A, Chiacchiera F, Grossi V, Matrone A, Latorre D, Simonatto M, Fusella A, Ryall JG, Finley LW, Haigis MC, Villani G, Puri PL, Sartorelli V, Simone C (2013) A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels. Cell Mol Life Sci 70:2015–2029
40. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, Capaldi RA (2004) Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 64:985–993
41. Sauer LA, Dauchy RT, Nagel WO, Morris HP (1980) Mitochondrial malic enzymes. Mitochondrial NAD(P) + −dependent malic enzyme activity and malate-dependent pyruvate formation are progression-linked in Morris hepatomas. J Biol Chem 255:3844–3848
42. Seagroves TN, Ryan HE, Lu H, Wouters BG, Knapp M, Thibault P, Laderoute K, Johnson RS (2001) Transcription factor HIF1 is necessary mediator of the Pasteur effect in mammalian cells. Mol Cell Biol 21:3436–3444
43. Semenza GL (2007) Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J 405:1–9
44. Semenza GL (2011) Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim Biophys Acta 1813:1263–1268
45. Semenza GL (2012a) Hypoxia-inducible factors in physiology and medicine. Cell 148:399–408
46. Semenza GL (2012b) Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci 33:207–214
47. Semenza GL (2013) HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations. J Clin Invest 123:3664–3671
48. Smolková K, Plecitá–Hlavatá L, Bellance N, Benard G, Rossignol R, Ježek P (2011) Waves of gene regulation suppress and then restore oxidative phosphorylation in cancer cells. Int J Biochem Cell Biol 43:950–968
49. Smolková K, Dvořák A, Zelenka J, Vítek L, Ježek P Reductive carboxylation and 2-hydroxyglutarate formation by wild–type IDH2 in breast carcinoma cells. Int J Biochem Cell Biol. 2015;47
50. Sookoian S, Pirola CJ (2012) Alanine and aspartate aminotransferase and glutamine-cycling pathway: their roles in pathogenesis of metabolic syndrome. World J Gastroenterol 18:3775–3781
51. Sun RC, Denko NC (2014) Hypoxic regulation of glutamine metabolism through HIF1 and SIAH2 supports lipid synthesis that is necessary for tumor growth. Cell Metab 19:285–292
52. Taylor CT (2008) Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J 409:19–26
53. Tong X, Zhao F, Mancuso A, Gruber JJ, Thompson CB (2009) The glucose-responsive transcription factor ChREBP contributes to glucose-dependent anabolic synthesis and cell proliferation. Proc Natl Acad Sci U S A 106:21660–21665
54. Vander Heiden MG, Locasale JW, Swanson KD, Sharfi H, Heffron GJ, Amador-Noguez D, Christofk HR, Wagner G, Rabinowitz JD, Asara JM, Cantley LC (2010) Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 329:1492–1499
55. Vaupel P, Höckel M, Mayer A (2007) Detection and characterization of tumor hypoxia using pO2 histography. Antioxid Redox Signal 9:1221–1235
56. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324:1076–1080
57. Wigfield SM, Winter SC, Giatromanolaki A, Taylor J, Koukourakis ML, Harris AL (2008) PDK-1 regulates lactate production in hypoxia and is associated with poor prognosis in head and neck squamous cancer. Br J Cancer 98:1975–1984
58. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK, Nissim I, Daikhin E, Yudkoff M, McMahon SB, Thompson CB (2008) Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci U S A 105:18782–18787
59. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, Parslow D, Armistead S, Lemire K, Orrell J, Teich J, Chomicz S, Ferrick DA (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 292:C125–C136
60. Yamashita H, Takenoscita M, Sakurai M, Bruick RK, Henzel WJ, Shillinglaw W, Arnot D, Uyeda K (2001) A glucose-responsive transcription factor that regulates carbohydrate metabolism in the liver. Proc Natl Acad Sci U S A 98:9116–9121
61. Yuneva M (2008) Finding an “Achilles’ heel” of cancer. Cell Cycle 7:2083–2089
62. Yuneva M, Zamboni N, Oefner P, Sachidanandam R, Lazebnik Y (2007) Deficiency in glutamine but not glucose induces MYC dependent apoptosis in human cells. J Cell Biol 178:93–105
63. Zepeda AB, Pessoa Jr A, Castillo RL, Figueroa CA, Pulgar VM, Farías JG (2013) Cellular and molecular mechanisms in the hypoxic tissue: role of HIF-1 and ROS. Cell Biochem Funct 31:451–459
64. Zhang Y, Yang JM (2013) Altered energy metabolism in cancer. A unique opportunity for the therapeutic intervention. Cancer Biol Ther 2:81–89
65. Zielke HR, Zielke CL, Ozand PT (1984) Glutamine: a major energy source for cultured mammalian cells. Fed Proc 43:121–125