Metabolic dysfunction consistent with premature aging results from deletion of pim kinases

Circulation Research

Volumn 115, Issue 3, 2014, Pages 376-387

  Din, Shabana ^a   Konstandin, Mathias H ^a   Johnson, Bevan ^a   Emathinger, Jacqueline ^a   Völkers, Mirko ^a   Toko, Haruhiro ^a   Collins, Brett ^a   Ormachea, Lucy ^a   Samse, Kaitlen ^a   Kubli, Dieter A ^b   De La Torre, Andrea ^a   Kraft, Andrew S ^c   Gustafsson, Asa B ^b   Kelly, Daniel P ^d   Sussman, Mark A ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d BURNHAM INSTITUTE   (United States)

Author keywords

aging; hypertrophy; metabolism; proto oncogene proteins pim

Indexed keywords

6 PHOSPHOFRUCTO 2 KINASE; 6 PHOSPHOFRUCTOKINASE; ACTIN; ADENOSINE TRIPHOSPHATE; ALPHA SKELETAL ACTIN; ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; CALSEQUESTRIN; CYCLOOXYGENASE 1; CYTOCHROME B; ESTROGEN RELATED RECEPTOR ALPHA; HEMOGLOBIN BETA CHAIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MYC PROTEIN; MYOSIN HEAVY CHAIN BETA; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PROTEIN KINASE B; PROTEIN KINASE PIM 1; PROTEIN KINASE PIM 2; PROTEIN KINASE PIM 3; PROTEIN MDM2; PROTEIN SERINE THREONINE KINASE; PYRUVATE DEHYDROGENASE KINASE 4; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; BIOGENESIS; BODY WEIGHT; CELL AGING; CELL ENERGY; CELL METABOLISM; CELL SIZE; CELL STRUCTURE; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; DETERIORATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ECHOCARDIOGRAPHY; ELECTRON MICROSCOPY; ENZYME PHOSPHORYLATION; FATTY ACID OXIDATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION; GLYCOLYSIS; HEART EJECTION FRACTION; HEART FAILURE; HEART FUNCTION; HEART INFARCTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART RATE; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; METABOLIC DISORDER; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; ONCOGENE C MYC; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PREMATURE AGING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TARGETING; SENESCENCE; TELOMERE; TRANSCRIPTION INITIATION; UPREGULATION; VIRAL GENE DELIVERY SYSTEM;

AGING; HYPERTROPHY; METABOLISM; PROTO-ONCOGENE PROTEINS PIM;

AGING, PREMATURE; ANIMALS; CARDIOMEGALY; CELL AGING; CELL LINE, TRANSFORMED; CELL RESPIRATION; FIBROBLASTS; HUMANS; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; PROTO-ONCOGENE PROTEINS C-MYC; PROTO-ONCOGENE PROTEINS C-PIM-1; RATS; RNA, SMALL INTERFERING; TELOMERE; TRANSCRIPTION FACTORS;

EID: 84904637755     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.304441     Document Type: Article

References (50)

1. Anversa P, Fitzpatrick D, Argani S, Capasso JM. Myocyte mitotic division in the aging mammalian rat heart. Circ Res. 1991;69:1159-1164.
2. Cesselli D, Beltrami AP, D'Aurizio F, et al. Effects of age and heart failure on human cardiac stem cell function. Am J Pathol. 2011;179:349-366.
3. Gonzalez A, Rota M, Nurzynska D, et al. Activation of cardiac progenitor cells reverses the failing heart senescent phenotype and prolongs lifespan. Circ Res. 2008;102:597-606.
4. Lai L, Leone TC, Zechner C, Schaeffer PJ, Kelly SM, Flanagan DP, Medeiros DM, Kovacs A, Kelly DP. Transcriptional coactivators PGC- 1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev. 2008;22:1948-1961.
5. Arany Z, He H, Lin J, et al. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005;1:259-271.
6. Lehman JJ, Kelly DP. Transcriptional activation of energy metabolic switches in the developing and hypertrophied heart. Clin Exp Pharmacol Physiol. 2002;29:339-345.
7. Wenz T. Regulation of mitochondrial biogenesis and PGC-1alpha under cellular stress. Mitochondrion. 2013;13:134-142.
8. Finkelstein J, Gray N, Heemels MT, Marte B, Nath D. Metabolism and disease. Nature. 2012;491:347.
9. Aubert G, Vega RB, Kelly DP. Perturbations in the gene regulatory pathways controlling mitochondrial energy production in the failing heart. Biochim Biophys Acta. 2013;1833:840-847.
10. Duncan JG, Fong JL, Medeiros DM, Finck BN, Kelly DP. Insulin-resistant heart exhibits a mitochondrial biogenic response driven by the peroxisome proliferator-activated receptor-alpha/PGC-1alpha gene regulatory pathway. Circulation. 2007;115:909-917.
11. Leone TC, Kelly DP. Transcriptional control of cardiac fuel metabolism and mitochondrial function. Cold Spring Harb Symp Quant Biol. 2011;76:175-182.
12. Kelly DP, Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 2004;18:357-368.
13. Riehle C, Wende AR, Zaha VG, et al. PGC-1? deficiency accelerates the transition to heart failure in pressure overload hypertrophy. Circ Res. 2011;109:783-793.
14. Lelliott CJ, Medina-Gomez G, Petrovic N, et al. Ablation of PGC-1beta results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol. 2006;4:e369.
15. Beharry Z, Mahajan S, Zemskova M, Lin YW, Tholanikunnel BG, Xia Z, Smith CD, Kraft AS. The Pim protein kinases regulate energy metabolism and cell growth. Proc Natl Acad Sci U S A. 2011;108:528-533.
16. Borillo GA, Mason M, Quijada P, et al. Pim-1 kinase protects mitochondrial integrity in cardiomyocytes. Circ Res. 2010;106:1265-1274.
17. Zhang Y, Wang Z, Li X, Magnuson NS. Pim kinase-dependent inhibition of c-Myc degradation. Oncogene. 2008;27:4809-4819.
18. Ahuja P, Zhao P, Angelis E, Ruan H, Korge P, Olson A, Wang Y, Jin ES, Jeffrey FM, Portman M, Maclellan WR. Myc controls transcriptional regulation of cardiac metabolism and mitochondrial biogenesis in response to pathological stress in mice. J Clin Invest. 2010;120:1494-1505.
19. Din S, Mason M, Völkers M, Johnson B, Cottage CT, Wang Z, Joyo AY, Quijada P, Erhardt P, Magnuson NS, Konstandin MH, Sussman MA. Pim- 1 preserves mitochondrial morphology by inhibiting dynamin-related protein 1 translocation. Proc Natl Acad Sci U S A. 2013;110:5969-5974.
20. Sussman MA. Mitochondrial integrity: preservation through Akt/Pim- 1 kinase signaling in the cardiomyocyte. Expert Rev Cardiovasc Ther. 2009;7:929-938.
21. Amaravadi R, Thompson CB. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest. 2005;115:2618-2624.
22. Muraski JA, Rota M, Misao Y, et al. Pim-1 regulates cardiomyocyte survival downstream of Akt. Nat Med. 2007;13:1467-1475.
23. Cottage CT, Neidig L, Sundararaman B, Din S, Joyo AY, Bailey B, Gude N, Hariharan N, Sussman MA. Increased mitotic rate coincident with transient telomere lengthening resulting from pim-1 overexpression in cardiac progenitor cells. Stem Cells. 2012;30:2512-2522.
24. Mohsin S, Khan M, Nguyen J, Alkatib M, Siddiqi S, Hariharan N, Wallach K, Monsanto M, Gude N, Dembitsky W, Sussman MA. Rejuvenation of human cardiac progenitor cells with Pim-1 kinase. Circ Res. 2013;113:1169-1179.
25. Mikkers H, Nawijn M, Allen J, Brouwers C, Verhoeven E, Jonkers J, Berns A. Mice deficient for all PIM kinases display reduced body size and impaired responses to hematopoietic growth factors. Mol Cell Biol. 2004;24:6104-6115.
26. Muraski JA, Fischer KM, Wu W, et al. Pim-1 kinase antagonizes aspects of myocardial hypertrophy and compensation to pathological pressure overload. Proc Natl Acad Sci U S A. 2008;105:13889-13894.
27. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest. 2000;106:847-856.
28. Konstandin MH, Toko H, Gastelum GM, Quijada P, De La Torre A, Quintana M, Collins B, Din S, Avitabile D, Völkers M, Gude N, Fässler R, Sussman MA. Fibronectin is essential for reparative cardiac progenitor cell response after myocardial infarction. Circ Res. 2013;113:115-125.
29. Konstandin MH, Völkers M, Collins B, Quijada P, Quintana M, De La Torre A, Ormachea L, Din S, Gude N, Toko H, Sussman MA. Fibronectin contributes to pathological cardiac hypertrophy but not physiological growth. Basic Res Cardiol. 2013;108:375.
30. Kubli DA, Zhang X, Lee Y, Hanna RA, Quinsay MN, Nguyen CK, Jimenez R, Petrosyan S, Murphy AN, Gustafsson AB. Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem. 2013;288:915-926.
31. Cawthon RM. Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res. 2009;37:e21.
32. Turdi S, Fan X, Li J, Zhao J, Huff AF, Du M, Ren J. AMP-activated protein kinase deficiency exacerbates aging-induced myocardial contractile dysfunction. Aging Cell. 2010;9:592-606.
33. Susic D, Frohlich ED. The aging hypertensive heart: a brief update. Nat Clin Pract Cardiovasc Med. 2008;5:104-110.
34. Fischer KM, Cottage CT, Konstandin MH, Völkers M, Khan M, Sussman MA. Pim-1 kinase inhibits pathological injury by promoting cardioprotective signaling. J Mol Cell Cardiol. 2011;51:554-558.
35. Chabowski A, Momken I, Coort SL, Calles-Escandon J, Tandon NN, Glatz JF, Luiken JJ, Bonen A. Prolonged AMPK activation increases the expression of fatty acid transporters in cardiac myocytes and perfused hearts. Mol Cell Biochem. 2006;288:201-212.
36. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell. 2013;153:1194-1217.
37. Iemitsu M, Miyauchi T, Maeda S, Tanabe T, Takanashi M, Irukayama- Tomobe Y, Sakai S, Ohmori H, Matsuda M, Yamaguchi I. Aging-induced decrease in the PPAR-alpha level in hearts is improved by exercise training. Am J Physiol Heart Circ Physiol. 2002;283:H1750-H1760.
38. Sihag S, Cresci S, Li AY, Sucharov CC, Lehman JJ. PGC-1alpha and ERRalpha target gene downregulation is a signature of the failing human heart. J Mol Cell Cardiol. 2009;46:201-212.
39. Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, Zeller KI, Dang CV, Semenza GL. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell. 2007;11:407-420.
40. Li F, Wang Y, Zeller KI, Potter JJ, Wonsey DR, O'Donnell KA, Kim JW, Yustein JT, Lee LA, Dang CV. Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Mol Cell Biol. 2005;25:6225-6234.
41. Chan DC. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet. 2012;46:265-287.
42. Karamanlidis G, Bautista-Hernandez V, Fynn-Thompson F, Del Nido P, Tian R. Impaired mitochondrial biogenesis precedes heart failure in right ventricular hypertrophy in congenital heart disease. Circ Heart Fail. 2011;4:707-713.
43. Sahin E, Colla S, Liesa M, et al. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature. 2011;470:359-365.
44. Kajstura J, Pertoldi B, Leri A, Beltrami CA, Deptala A, Darzynkiewicz Z, Anversa P. Telomere shortening is an in vivo marker of myocyte replication and aging. Am J Pathol. 2000;156:813-819.
45. Kajstura J, Gurusamy N, Ogórek B, et al. Myocyte turnover in the aging human heart. Circ Res. 2010;107:1374-1386.
46. Kajstura J, Rota M, Cappetta D, et al. Cardiomyogenesis in the aging and failing human heart. Circulation. 2012;126:1869-1881.
47. Mochizuki T, Kitanaka C, Noguchi K, Muramatsu T, Asai A, Kuchino Y. Physical and functional interactions between Pim-1 kinase and Cdc25A phosphatase. Implications for the Pim-1-mediated activation of the c-Myc signaling pathway. J Biol Chem. 1999;274:18659-18666.
48. Morishita D, Katayama R, Sekimizu K, Tsuruo T, Fujita N. Pim kinases promote cell cycle progression by phosphorylating and down-regulating p27Kip1 at the transcriptional and posttranscriptional levels. Cancer Res. 2008;68:5076-5085.
49. Zhang Y, Wang Z, Magnuson NS. Pim-1 kinase-dependent phosphorylation of p21Cip1/WAF1 regulates its stability and cellular localization in H1299 cells. Mol Cancer Res. 2007;5:909-922.
50. Lee HC, Wei YH. Mitochondria and aging. Adv Exp Med Biol. 2012;942:311-327.