PDK4 Inhibits Cardiac Pyruvate Oxidation in Late Pregnancy

Circulation Research

Volumn 121, Issue 12, 2017, Pages 1370-1378

  Liu, Laura X ^a,b   Rowe, Glenn C ^a,c   Yang, Steven ^d   Li, Jian ^d   Damilano, Federico ^b   Chan, Mun Chun ^b   Lu, Wenyun ^e   Jang, Cholsoon ^e   Wada, Shogo ^d   Morley, Michael ^d   Hesse, Michael ^f   Fleischmann, Bernd K ^f   Rabinowitz, Joshua D ^e   Das, Saumya ^b   Rosenzweig, Anthony ^b   Arany, Zoltan ^a,d  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e PRINCETON UNIVERSITY   (United States)

^f UNIVERSITY OF BONN   (Germany)

Author keywords

glucose; heart; metabolism; mitochondria; pregnancy; progesterone

Indexed keywords

CARBON 13; CD36 ANTIGEN; FATTY ACID; FATTY ACID TRANSPORTER; GLUCOSE; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 4; LACTIC ACID; PROGESTERONE; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE 4; PYRUVIC ACID; TRACER; PROTEIN SERINE THREONINE KINASE; PYRUVATE DEHYDROGENASE (ACETYL-TRANSFERRING) KINASE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CITRIC ACID CYCLE; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME INHIBITION; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; FEMALE; GLUCOSE OXIDATION; HEART MUSCLE METABOLISM; INSULIN SIGNALING; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; THIRD TRIMESTER PREGNANCY; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; METABOLISM; PREGNANCY;

ANIMALS; CITRIC ACID CYCLE; FATTY ACIDS; FEMALE; GLUCOSE; LACTIC ACID; MICE; MICE, INBRED C57BL; MYOCARDIUM; PREGNANCY; PROGESTERONE; PROTEIN-SERINE-THREONINE KINASES; PYRUVIC ACID;

EID: 85037073639     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.117.311456     Document Type: Article

References (41)

1. Lain KY, Catalano PM. Metabolic changes in pregnancy. Clin Obstet Gynecol. 2007;50:938-948. doi: 10.1097/GRF.0b013e31815a5494.
2. Barbour LA, McCurdy CE, Hernandez TL, Kirwan JP, Catalano PM, Friedman JE. Cellular mechanisms for insulin resistance in normal pregnancy, gestational diabetes. Diabetes Care. 2007;30(suppl 2):S112-S119. doi: 10.2337/dc07-s202.
3. Kirwan JP, Hauguel-De Mouzon S, Lepercq J, Challier JC, Huston-Presley L, Friedman JE, Kalhan SC, Catalano PM. TNF-alpha is a predictor of insulin resistance in human pregnancy. Diabetes. 2002;51:2207-2213.
4. Melchiorre K, Sharma R, Thilaganathan B. Cardiac structure, function in normal pregnancy. Curr Opin Obstet Gynecol. 2012;24:413-421. doi: 10.1097/GCO.0b013e328359826f.
5. Chung E, Leinwand LA. Pregnancy as a cardiac stress model. Cardiovasc Res. 2014;101:561-570. doi: 10.1093/cvr/cvu013.
6. Liu LX, Arany Z. Maternal cardiac metabolism in pregnancy. Cardiovasc Res. 2014;101:545-553. doi: 10.1093/cvr/cvu009.
7. Sugden MC, Changani KK, Bentley J, Holness MJ. Cardiac glucose metabolism during pregnancy. Biochem Soc Trans. 1992;20:195S.
8. Sugden MC, Holness MJ. Cardiac carbohydrate, lipid utilization during late pregnancy. Biochem Soc Trans. 1993;21(pt 3):312S.
9. Sugden MC, Holness MJ. Control of muscle pyruvate oxidation during late pregnancy. FEBS Lett. 1993;321:121-126.
10. Williams JG, Ojaimi C, Qanud K, Zhang S, Xu X, Recchia FA, Hintze TH. Coronary nitric oxide production controls cardiac substrate metabolism during pregnancy in the dog. Am J Physiol Heart Circ Physiol. 2008;294:H2516-H2523. doi: 10.1152/ajpheart.01196.2007.
11. Williams JG, Rincon-Skinner T, Sun D, Wang Z, Zhang S, Zhang X, Hintze TH. Role of nitric oxide in the coupling of myocardial oxygen consumption, coronary vascular dynamics during pregnancy in the dog. Am J Physiol Heart Circ Physiol. 2007;293:H2479-H2486. doi: 10.1152/ajpheart.00036.2006.
12. Chung E, Yeung F, Leinwand LA. Akt, MAPK signaling mediate pregnancy-induced cardiac adaptation. J Appl Physiol. 2012;112:1564-1575. doi: 10.1152/japplphysiol.00027.2012.
13. Hilfiker-Kleiner D, Kaminski K, Podewski E, et al. A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. Cell. 2007;128:589-600. doi: 10.1016/j.cell.2006.12.036.
14. Lemmens K, Doggen K, De Keulenaer GW. Activation of the neuregulin/ErbB system during physiological ventricular remodeling in pregnancy. Am J Physiol Heart Circ Physiol. 2011;300:H931-H942. doi: 10.1152/ajpheart.00385.2010.
15. Buescher JM, Antoniewicz MR, Boros LG, et al. A roadmap for interpreting (13)C metabolite labeling patterns from cells. Curr Opin Biotechnol. 2015;34:189-201. doi: 10.1016/j.copbio.2015.02.003.
16. Murray SA, Morgan JL, Kane C, Sharma Y, Heffner CS, Lake J, Donahue LR. Mouse gestation length is genetically determined. PLoS One. 2010;5:e12418. doi: 10.1371/journal.pone.0012418.
17. Henkin AH, Cohen AS, Dubikovskaya EA, Park HM, Nikitin GF, Auzias MG, Kazantzis M, Bertozzi CR, Stahl A. Real-time noninvasive imaging of fatty acid uptake in vivo. ACS Chem Biol. 2012;7:1884-1891. doi: 10.1021/cb300194b.
18. Wharfe MD, Wyrwoll CS, Waddell BJ, Mark PJ. Pregnancy-induced changes in the circadian expression of hepatic clock genes: Implications for maternal glucose homeostasis. Am J Physiol Endocrinol Metab. 2016;311:E575-E586. doi: 10.1152/ajpendo.00060.2016.
19. Sugiyama C, Yamamoto M, Kotani T, Kikkawa F, Murata Y, Hayashi Y. Fertility, pregnancy-associated-cell proliferation in mice deficient in proglucagon-derived peptides. PLoS One. 2012;7:e43745. doi: 10.1371/journal.pone.0043745.
20. Goddard LM, Murphy TJ, Org T, et al. Progesterone receptor in the vascular endothelium triggers physiological uterine permeability preimplantation. Cell. 2014;156:549-562. doi: 10.1016/j.cell.2013.12.025.
21. Tyner C, Barber GP, Casper J, et al. The UCSC Genome Browser database: 2017 update. Nucleic Acids Res. 2017;45:D626-D634. doi: 10.1093/nar/gkw1134.
22. Yin P, Roqueiro D, Huang L, Owen JK, Xie A, Navarro A, Monsivais D, Coon JS V, Kim JJ, Dai Y, Bulun SE. Genome-wide progesterone receptor binding: Cell type-specific, shared mechanisms in T47D breast cancer cells, primary leiomyoma cells. PLoS One. 2012;7:e29021. doi: 10.1371/journal.pone.0029021.
23. Grundberg E, Small KS, Hedman ÅK, et al; Multiple Tissue Human Expression Resource (MuTHER) Consortium. Mapping cis-, trans-regulatory effects across multiple tissues in twins. Nat Genet. 2012;44:1084-1089. doi: 10.1038/ng.2394.
24. Yu CH, Pal LR, Moult J. Consensus genome-wide expression quantitative trait loci, their relationship with human complex trait disease. OMICS. 2016;20:400-414. doi: 10.1089/omi.2016.0063.
25. Bersin RM, Stacpoole PW. Dichloroacetate as metabolic therapy for myocardial ischemia, failure. Am Heart J. 1997;134:841-855.
26. Rimbaud S, Sanchez H, Garnier A, Fortin D, Bigard X, Veksler V, Ventura-Clapier R. Stimulus specific changes of energy metabolism in hypertrophied heart. J Mol Cell Cardiol. 2009;46:952-959.
27. Redondo-Angulo I, Mas-Stachurska A, Sitges M, Giralt M, Villarroya F, Planavila A. C/EBP is required in pregnancy-induced cardiac hypertrophy. Int J Cardiol. 2016;202:819-828. doi: 10.1016/j. ijcard.2015.10.005.
28. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fattyacid cycle. Its role in insulin sensitivity, the metabolic disturbances of diabetes mellitus. Lancet. 1963;1:785-789.
29. Hue L, Taegtmeyer H. The Randle cycle revisited: A new head for an old hat. Am J Physiol Endocrinol Metab. 2009;297:E578-E591. doi: 10.1152/ajpendo.00093.2009.
30. Randle PJ, Sugden PH, Kerbey AL, Radcliffe PM, Hutson NJ. Regulation of pyruvate oxidation, the conservation of glucose. Biochem Soc Symp. 1978;43:47-67.
31. Campbell SE, Mehan KA, Tunstall RJ, Febbraio MA, Cameron-Smith D. 17beta-estradiol upregulates the expression of peroxisome proliferatoractivated receptor alpha, lipid oxidative genes in skeletal muscle. J Mol Endocrinol. 2003;31:37-45.
32. Morrissy S, Xu B, Aguilar D, Zhang J, Chen QM. Inhibition of apoptosis by progesterone in cardiomyocytes. Aging Cell. 2010;9:799-809. doi: 10.1111/j.1474-9726.2010.00619.x.
33. Nakamura H, Kurokawa J, Bai CX, Asada K, Xu J, Oren RV, Zhu ZI, Clancy CE, Isobe M, Furukawa T. Progesterone regulates cardiac repolarization through a nongenomic pathway: An in vitro patch-clamp, computational modeling study. Circulation. 2007;116:2913-2922. doi: 10.1161/CIRCULATIONAHA.107.702407.
34. Wittnich C, Tan L, Wallen J, Belanger M. Sex differences in myocardial metabolism, cardiac function: An emerging concept. Pflugers Arch. 2013;465:719-729. doi: 10.1007/s00424-013-1232-1.
35. Bello NA, Arany Z. Molecular mechanisms of peripartum cardiomyopathy: A vascular/hormonal hypothesis. Trends Cardiovasc Med. 2015;25:499-504. doi: 10.1016/j.tcm.2015.01.004.
36. Arany Z, Elkayam U. Peripartum cardiomyopathy. Circulation. 2016;133:1397-1409. doi: 10.1161/CIRCULATIONAHA.115.020491.
37. Patten IS, Rana S, Shahul S, et al. Cardiac angiogenic imbalance leads to peripartum cardiomyopathy. Nature. 2012;485:333-338. doi: 10.1038/nature11040.
38. Rowe GC, Jiang A, Arany Z. PGC-1 coactivators in cardiac development, disease. Circ Res. 2010;107:825-838. doi: 10.1161/CIRCRESAHA.110.223818.
39. Wende AR, Huss JM, Schaeffer PJ, Giguère V, Kelly DP. PGC-1alpha coactivates PDK4 gene expression via the orphan nuclear receptor ERRalpha: A mechanism for transcriptional control of muscle glucose metabolism. Mol Cell Biol. 2005;25:10684-10694. doi: 10.1128/MCB.25.24.10684-10694.2005.
40. Bello N, Rendon IS, Arany Z. The relationship between pre-eclampsia, peripartum cardiomyopathy: A systematic review, metaanalysis. J Am Coll Cardiol. 2013;62:1715-1723. doi: 10.1016/j. jacc.2013.08.717.
41. Powe CE, Levine RJ, Karumanchi SA. Preeclampsia, a disease of the maternal endothelium: The role of antiangiogenic factors, implications for later cardiovascular disease. Circulation. 2011;123:2856-2869. doi: 10.1161/CIRCULATIONAHA.109.853127.