CAPER Is Vital for Energy and Redox Homeostasis by Integrating Glucose-Induced Mitochondrial Functions via ERR-α-Gabpa and Stress-Induced Adaptive Responses via NF-κB-cMYC

English version České info

Energy homeostasis is a vital prerequisite for optimal nutrient utilization and prolonged survival in an environment with fluctuating and frequently scarce food resources. Numerous studies have elucidated the important roles of mitochondrial energy in fasting status but less is known about the role of mitochondria in fed status. Two recent studies elucidated the importance of nutrient-induced mitochondrial functions [1,2] in mammalian longevity, but these studies did not either address how these critical nutrient-induced mitochondrial functions are integrated with nutrient-enhanced antioxidant capacities—nor identify how the carbon and nitrogen balance is maintained. Our study reveals CAPER, as the `first’ example of a coregulator nodal integrator which eukaryotes share to orchestrate both nutrient-induced mitochondrial energy metabolism by coactivating ERR-α-Gabpa and stress-induced adaptive metabolic responses via NF -⁠ κB/c-Myc; this allows maintenance of carbon-nitrogen balance as well as preservation of life span and reproductive capacity. These metabolic roles for the CAPER coactivator in energy homeostasis are highly conserved and crucial for life span and reproduction in human cells and C. elegans.

Vyšlo v časopise: CAPER Is Vital for Energy and Redox Homeostasis by Integrating Glucose-Induced Mitochondrial Functions via ERR-α-Gabpa and Stress-Induced Adaptive Responses via NF-κB-cMYC. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005116
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005116

Souhrn

Zdroje

1. Gomes AP, Price NL, Ling AJ, Moslehi JJ, Montgomery MK, et al. (2013) Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155 : 1624–1638. doi: 10.1016/j.cell.2013.11.037 24360282

2. Solon-Biet SM, McMahon AC, Ballard JW, Ruohonen K, Wu LE, et al. (2014) The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab 19 : 418–430. doi: 10.1016/j.cmet.2014.02.009 24606899

3. Jung DJ, Na SY, Na DS, Lee JW (2002) Molecular cloning and characterization of CAPER, a novel coactivator of activating protein-1 and estrogen receptors. J Biol Chem 277 : 1229–1234. 11704680

4. Dowhan DH, Hong EP, Auboeuf D, Dennis AP, Wilson MM, et al. (2005) Steroid hormone receptor coactivation and alternative RNA splicing by U2AF65-related proteins CAPERalpha and CAPERbeta. Mol Cell 17 : 429–439. 15694343

5. Mercier I, Casimiro MC, Zhou J, Wang C, Plymire C, et al. (2009) Genetic Ablation of Caveolin-1 Drives Estrogen-Hypersensitivity and the Development of DCIS-Like Mammary Lesions. The American Journal of Pathology 174 : 1172–1190. doi: 10.2353/ajpath.2009.080882 19342371

6. Dutta J, Fan G, Gélinas C (2008) CAPERα Is a Novel Rel-TAD-Interacting Factor That Inhibits Lymphocyte Transformation by the Potent Rel/NF-κB Oncoprotein v-Rel. Journal of Virology 82 : 10792–10802. doi: 10.1128/JVI.00903-08 18753212

7. Wu JC, Merlino G, Fausto N (1994) Establishment and characterization of differentiated, nontransformed hepatocyte cell lines derived from mice transgenic for transforming growth factor alpha. Proceedings of the National Academy of Sciences 91 : 674–678. 7904757

8. Zhou J, Tan S-H, Nicolas V, Bauvy C, Yang N-D, et al. (2013) Activation of lysosomal function in the course of autophagy via mTORC1 suppression and autophagosome-lysosome fusion. Cell Res 23 : 508–523. doi: 10.1038/cr.2013.11 23337583

9. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8 : 445–544. 22966490

10. Finck BN, Kelly DP (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 116 : 615–622. 16511594

11. Chopra AR, Kommagani R, Saha P, Louet JF, Salazar C, et al. Cellular energy depletion resets whole-body energy by promoting coactivator-mediated dietary fuel absorption. Cell Metab 13 : 35–43. doi: 10.1016/j.cmet.2010.12.001 21195347

12. Bensaad K, Vousden KH (2007) p53: new roles in metabolism. Trends in Cell Biology 17 : 286–291. 17481900

13. Villeneuve NF, Sun Z, Chen W, Zhang DD (2009) Nrf2 and p21 regulate the fine balance between life and death by controlling ROS levels. Cell Cycle 8 : 3255–3256. 19806015

14. Lee J, Giordano S, Zhang J (2012) Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441 : 523–540. doi: 10.1042/BJ20111451 22187934

15. Owusu-Ansah E, Yavari A, Mandal S, Banerjee U (2008) Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat Genet 40 : 356–361. doi: 10.1038/ng.2007.50 18246068

16. Scarpulla RC (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann N Y Acad Sci 1147 : 321–334. doi: 10.1196/annals.1427.006 19076454

17. Jazwinski SM (2013) The retrograde response: when mitochondrial quality control is not enough. Biochim Biophys Acta 1833 : 400–409. doi: 10.1016/j.bbamcr.2012.02.010 22374136

18. Sreekumar A, Poisson LM, Rajendiran TM, Khan AP, Cao Q, et al. (2009) Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature 457 : 910–914. doi: 10.1038/nature07762 19212411

19. Putluri N, Shojaie A, Vasu VT, Vareed SK, Nalluri S, et al. (2011) Metabolomic profiling reveals potential markers and bioprocesses altered in bladder cancer progression. Cancer Res 71 : 7376–7386. doi: 10.1158/0008-5472.CAN-11-1154 21990318

20. Valcourt JR, Lemons JM, Haley EM, Kojima M, Demuren OO, et al. (2012) Staying alive: metabolic adaptations to quiescence. Cell Cycle 11 : 1680–1696. doi: 10.4161/cc.19879 22510571

21. Harnisch JM, Harnisch PH, Harnisch DR Sr (2012) Family Medicine Obstetrics: Pregnancy and Nutrition. Primary Care: Clinics in Office Practice 39 : 39–54. doi: 10.1016/j.pop.2011.11.003 22309580

22. Della Torre S, Rando G, Meda C, Stell A, Chambon P, et al. Amino Acid-Dependent Activation of Liver Estrogen Receptor Alpha Integrates Metabolic and Reproductive Functions via IGF-1. Cell Metabolism 13 : 205–214. doi: 10.1016/j.cmet.2011.01.002 21284987

23. Michalakis K, Mintziori G, Kaprara A, Tarlatzis BC, Goulis DG (2013) The complex interaction between obesity, metabolic syndrome and reproductive axis: A narrative review. Metabolism.

24. Della Torre S, Rando G, Meda C, Stell A, Chambon P, et al. (2011) Amino acid-dependent activation of liver estrogen receptor alpha integrates metabolic and reproductive functions via IGF-1. Cell Metab 13 : 205–214. doi: 10.1016/j.cmet.2011.01.002 21284987

25. Klosinska MM, Crutchfield CA, Bradley PH, Rabinowitz JD, Broach JR (2011) Yeast cells can access distinct quiescent states. Genes Dev 25 : 336–349. doi: 10.1101/gad.2011311 21289062

26. Levine ME, Suarez JA, Brandhorst S, Balasubramanian P, Cheng CW, et al. (2014) Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population. Cell Metab 19 : 407–417. doi: 10.1016/j.cmet.2014.02.006 24606898

27. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, et al. (2009) Caloric Restriction Delays Disease Onset and Mortality in Rhesus Monkeys. Science 325 : 201–204. doi: 10.1126/science.1173635 19590001

28. Mitro N, Mak PA, Vargas L, Godio C, Hampton E, et al. (2007) The nuclear receptor LXR is a glucose sensor. Nature 445 : 219–223. 17187055

29. Duran-Sandoval D, Mautino G, Martin G, Percevault F, Barbier O, et al. (2004) Glucose regulates the expression of the farnesoid X receptor in liver. Diabetes 53 : 890–898. 15047603

30. Briata P, Laurino C, Gherzi R (1989) c-myc Gene expression in human cells is controlled by glucose. Biochemical and Biophysical Research Communications 165 : 1123–1129. 2558650

31. Li MV, Chen W, Harmancey RN, Nuotio-Antar AM, Imamura M, et al. (2010) Glucose-6-phosphate mediates activation of the carbohydrate responsive binding protein (ChREBP). Biochem Biophys Res Commun 395 : 395–400. doi: 10.1016/j.bbrc.2010.04.028 20382127

32. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, et al. (2001) Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413 : 131–138. 11557972

33. Sillars-Hardebol AH, Carvalho B, Belien JA, de Wit M, Delis-van Diemen PM, et al. (2012) CSE1L, DIDO1 and RBM39 in colorectal adenoma to carcinoma progression. Cell Oncol (Dordr) 35 : 293–300. doi: 10.1007/s13402-012-0088-2 22711543

34. Ramakrishna M, Williams LH, Boyle SE, Bearfoot JL, Sridhar A, et al. (2010) Identification of candidate growth promoting genes in ovarian cancer through integrated copy number and expression analysis. PLoS One 5: e9983. doi: 10.1371/journal.pone.0009983 20386695

35. Ding Z, Wu C-J, Chu GC, Xiao Y, Ho D, et al. (2011) SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 470 : 269–273. doi: 10.1038/nature09677 21289624

36. Amazit L, Pasini L, Szafran AT, Berno V, Wu RC, et al. (2007) Regulation of SRC-3 intercompartmental dynamics by estrogen receptor and phosphorylation. Mol Cell Biol 27 : 6913–6932. 17646391

37. Kang YK, Schiff R, Ko L, Wang T, Tsai SY, et al. (2008) Dual roles for coactivator activator and its counterbalancing isoform coactivator modulator in human kidney cell tumorigenesis. Cancer Res 68 : 7887–7896. doi: 10.1158/0008-5472.CAN-08-1734 18829545

38. McLean-Bennett LoA (2011) Densitometry of Western blots using Image J Software.