Tafazzin knockdown interrupts cell cycle progression in cultured neonatal ventricular fibroblasts

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 9, 2013, Pages

  He, Quan ^a,b   Wang, Miao ^a   Harris, Nicole ^a   Han, Xianlin ^a  

^a BURNHAM INSTITUTE   (United States)

^b HENRY FORD HOSPITAL   (United States)

Author keywords

Cardiolipin; Cell cycle; Mitogen activated protein kinase; Reactive oxygen species

Indexed keywords

ADENOVIRUS VECTOR; CARDIOLIPIN; COLLAGEN; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PLASMID DNA; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; TAFAZZIN PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; BARTH SYNDROME; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONGESTIVE CARDIOMYOPATHY; DNA SYNTHESIS; ENZYME ACTIVATION; FIBROBLAST; GENE SILENCING; GENETIC TRANSFECTION; HEART MUSCLE CELL; NEONATAL VENTRICULAR FIBROBLAST; NONHUMAN; PRIORITY JOURNAL; RAT; VIRUS EXPRESSION;

CARDIOLIPIN; CELL CYCLE; MITOGEN-ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN SPECIES;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, NEWBORN; BARTH SYNDROME; CARDIOLIPINS; CARDIOMYOPATHY, DILATED; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; DNA REPLICATION; DOWN-REGULATION; ENZYME ACTIVATION; FIBROBLASTS; FIBROSIS; GENE KNOCKDOWN TECHNIQUES; HEART VENTRICLES; MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC; TRANSFECTION;

EID: 84887011625     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00084.2013     Document Type: Article

References (77)

1. Acehan D, Vaz F, Houtkooper RH, James J, Moore V, Tokunaga C, Kulik W, Wansapura J, Toth MJ, Strauss A, Khuchua Z. Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome. J Biol Chem 286: 899-908, 2011.
2. Agocha AE, Eghbali-Webb M. A simple method for preparation of cultured cardiac fibroblasts from adult human ventricular tissue. Mol Cell Biochem 172: 195-198, 1997.
3. Banerjee I, Yekkala K, Borg TK, Baudino TA. Dynamic interactions between myocytes, fibroblasts, and extracellular matrix. Ann N Y Acad Sci 1080: 76-84, 2006.
4. Banko MR, Allen JJ, Schaffer BE, Wilker EW, Tsou P, White JL, Villen J, Wang B, Kim SR, Sakamoto K, Gygi SP, Cantley LC, Yaffe MB, Shokat KM, Brunet A. Chemical genetic screen for AMPK alpha 2 substrates uncovers a network of proteins involved in mitosis. Mol Cell 44: 878-892, 2011.
5. Banks MF, Gerasimovskaya EV, Tucker DA, Frid MG, Carpenter TC, Stenmark KR. Egr-1 antisense oligonucleotides inhibit hypoxiainduced proliferation of pulmonary artery adventitial fibroblasts. J Appl Physiol 98: 732-738, 2005.
6. Barth PG, Valianpour F, Bowen VM, Lam J, Duran M, Vaz FM, Wanders RJ. X-linked cardioskeletal myopathy and neutropenia (Barth syndrome): an update. Am J Med Genet A 126A: 349-354, 2004.
7. Barth PG, Van den Bogert C, Bolhuis PA, Scholte HR, van Gennip AH, Schutgens RB, Ketel AG. X-linked cardioskeletal myopathy and neutropenia (Barth syndrome): respiratory-chain abnormalities in cultured fibroblasts. J Inherit Metab Dis 19: 157-160, 1996.
8. Berrebi D, Leclerc J, Schleiermacher G, Zaccaria I, Boccon-Gibod L, Fabre M, Jaubert F, El Ghoneimi A, Jeanpierre C, Peuchmaur M. High cyclin E staining index in blastemal, stromal or epithelial cells is correlated with tumor aggressiveness in patients with nephroblastoma. PLos One 3: e2216, 2008.
9. Booz GW, Baker KM. Molecular signalling mechanisms controlling growth and function of cardiac fibroblasts. Cardiovasc Res 30: 537-543, 1995.
10. Camelliti P, Borg TK, Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res 65: 40-51, 2005.
11. Chan AY, Soltys CL, Young ME, Proud CG, Dyck JR. Activation of AMP-activated protein kinase inhibits protein synthesis associated with hypertrophy in the cardiac myocyte. J Biol Chem 279: 32771-32779, 2004.
12. Chen S, He Q, Greenberg ML. Loss of tafazzin in yeast leads to increased oxidative stress during respiratory growth. Mol Microbiol 68: 1061-1072, 2008.
13. Chicco AJ, Sparagna GC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 292: C33-C44, 2007.
14. Chou MM, Masuda-Robens JM, Gupta ML. Cdc42 promotes G1 progression through p70 S6 kinase-mediated induction of cyclin E expression. J Biol Chem 278: 35241-35247, 2003.
15. Claypool SM, Boontheung P, McCaffery JM, Loo JA, Koehler CM. The cardiolipin transacylase, tafazzin, associates with two distinct respiratory components providing insight into Barth syndrome. Mol Biol Cell 19: 5143-5155, 2008.
16. Claypool SM, Whited K, Srijumnong S, Han X, Koehler CM. Barth syndrome mutations that cause tafazzin complex lability. J Cell Biol 192: 447-462, 2011.
17. Cortez DM, Feldman MD, Mummidi S, Valente AJ, Steffensen B, Vincenti M, Barnes JL, Chandrasekar B. IL-17 stimulates MMP-1 expression in primary human cardiac fibroblasts via p38 MAPK-and ERK1/2-dependent C/EBP-β, NF-B, and AP-1 activation. Am J Physiol Heart Circ Physiol 293: H3356-H3365, 2007.
18. Cui H, Kong Y, Zhang H. Oxidative stress, mitochondrial dysfunction, and aging. J Signal Transduct 2012: 1-13, 2012.
19. Dagon Y, Hur E, Zheng B, Wellenstein K, Cantley LC, Kahn BB. p70S6 kinase phosphorylates AMPK on serine 491 to mediate leptin's effect on food intake. Cell Metab 16: 104-112, 2012.
20. Decker T, Hipp S, Ringshausen I, Bogner C, Oelsner M, Schneller F, Peschel C. Rapamycin-induced G1 arrest in cycling B-CLL cells is associated with reduced expression of cyclin D3, cyclin E, cyclin A, and survivin. Blood 101: 278-285, 2003.
21. Dietrich DR. Toxicological and pathological applications of proliferating cell nuclear antigen (PCNA), a novel endogenous marker for cell proliferation. Crit Rev Toxicol 23: 77-109, 1993.
22. Freed DH, Moon MC, Borowiec AM, Jones SC, Zahradka P, Dixon IM. Cardiotrophin-1: expression in experimental myocardial infarction and potential role in post-MI wound healing. Mol Cell Biochem 254: 247-256, 2003.
23. Galati D, Srinivasan S, Raza H, Prabu SK, Hardy M, Chandran K, Lopez M, Kalyanaraman B, Avadhani NG. Role of nuclear-encoded subunit Vb in the assembly and stability of cytochrome c oxidase complex: implications in mitochondrial dysfunction and ROS production. Biochem J 420: 439-449, 2009.
24. Garnovskaya MN, Mukhin YV, Vlasova TM, Grewal JS, Ullian ME, Tholanikunnel BG, Raymond JR. Mitogen-induced rapid phosphorylation of serine 795 of the retinoblastoma gene product in vascular smooth muscle cells involves ERK activation. J Biol Chem 279: 24899-24905, 2004.
25. Gerasimovskaya EV, Tucker DA, Weiser-Evans M, Wenzlau JM, Klemm DJ, Banks M, Stenmark KR. Extracellular ATP-induced proliferation of adventitial fibroblasts requires phosphoinositide 3-kinase, Akt, mammalian target of rapamycin, and p70 S6 kinase signaling pathways. J Biol Chem 280: 1838-1848, 2005.
26. Green AS, Chapuis N, Maciel TT, Willems L, Lambert M, Arnoult C, Boyer O, Bardet V, Park S, Foretz M, Viollet B, Ifrah N, Dreyfus F, Hermine O, Moura IC, Lacombe C, Mayeux P, Bouscary D, Tamburini J. The LKB1/AMPK signaling pathway has tumor suppressor activity in acute myeloid leukemia through the repression of mTORdependent oncogenic mRNA translation. Blood 116: 4262-4273, 2010.
27. Grim JE, Clurman BE. Cycling without CDK2? Trends Cell Biol 13: 396-399, 2003.
28. Gu Z, Valianpour F, Chen S, Vaz FM, Hakkaart GA, Wanders RJ, Greenberg ML. Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome. Mol Microbiol 51: 149-158, 2004.
29. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30: 214-226, 2008.
30. Han MJ, Kim BY, Yoon SO, Chung AS. Cell proliferation induced by reactive oxygen species is mediated via mitogen-activated protein kinase in Chinese hamster lung fibroblast (V79) cells. Mol Cells 15: 94-101, 2003.
31. Han X, Yang K, Yang J, Cheng H, Gross RW. Shotgun lipidomics of cardiolipin molecular species in lipid extracts of biological samples. J Lipid Res 47: 864-879, 2006.
32. Harbour JW, Dean DC. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 14: 2393-2409, 2000.
33. Hauff K, Linda D, Hatch GM. Mechanism of the elevation in cardiolipin during HeLa cell entry into the S-phase of the human cell cycle. Biochem J 417: 573-582, 2009.
34. He Q. Tafazzin knockdown causes hypertrophy of neonatal ventricular myocytes. Am J Physiol Heart Circ Physiol 299: H210-H216, 2010.
35. Igata M, Motoshima H, Tsuruzoe K, Kojima K, Matsumura T, Kondo T, Taguchi T, Nakamaru K, Yano M, Kukidome D, Matsumoto K, Toyonaga T, Asano T, Nishikawa T, Araki E. Adenosine monophosphate-activated protein kinase suppresses vascular smooth muscle cell proliferation through the inhibition of cell cycle progression. Circ Res 97: 837-844, 2005.
36. Jiang F, Ryan MT, Schlame M, Zhao M, Gu Z, Klingenberg M, Pfanner N, Greenberg ML. Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J Biol Chem 275: 22387-22394, 2000.
37. Kalavakunta JK, Tokala H, Gosavi A, Gupta V. Left ventricular noncompaction and myocardial fibrosis: a case report. Int Arch Med. In press.
38. Kanazawa S, Fujiwara Y, Mizuno K. Selective repression of growthregulating cdk2, cyclin E and E2F1 genes in human cell senescence. Kobe J Med Sci 40: 165-174, 1994.
39. Kanda S, Hodgkin MN, Woodfield RJ, Wakelam MJ, Thomas G, Claesson-Welsh L. Phosphatidylinositol 3=-kinase-independent p70 S6 kinase activation by fibroblast growth factor receptor-1 is important for proliferation but not differentiation of endothelial cells. J Biol Chem 272: 23347-23353, 1997.
40. Khuchua Z, Yue Z, Batts L, Strauss AW. A zebrafish model of human Barth syndrome reveals the essential role of tafazzin in cardiac development and function. Circ Res 99: 201-208, 2006.
41. Kiebish MA, Yang K, Sims HF, Jenkins CM, Liu X, Mancuso DJ, Zhao Z, Guan S, Abendschein DR, Han X, Gross RW. Myocardial regulation of lipidomic flux by cardiolipin synthase: setting the beat for bioenergetic efficiency. J Biol Chem 287: 25086-25097, 2012.
42. Koff A, Giordano A, Desai D, Yamashita K, Harper JW, Elledge S, Nishimoto T, Morgan DO, Franza BR, Roberts JM. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257: 1689-1694, 1992.
43. Krenning G, Zeisberg EM, Kalluri R. The origin of fibroblasts and mechanism of cardiac fibrosis. J Cell Physiol 225: 631-637, 2010.
44. Kulik W, van Lenthe H, Stet FS, Houtkooper RH, Kemp H, Stone JE, Steward CG, Wanders RJ, Vaz FM. Bloodspot assay using HPLCtandem mass spectrometry for detection of Barth syndrome. Clin Chem 54: 371-378, 2008.
45. Li PF, Dietz R, von Harsdorf R. Superoxide induces apoptosis in cardiomyocytes, but proliferation and expression of transforming growth factor-beta1 in cardiac fibroblasts. FEBS Lett 448: 206-210, 1999.
46. Liang Y, Gao H, Lin SY, Goss JA, Brunicardi FC, Li K. siRNA-based targeting of cyclin E overexpression inhibits breast cancer cell growth and suppresses tumor development in breast cancer mouse model. PLos One 5: e12860, 2010.
47. Ling MT, Wang X, Ouyang XS, Lee TK, Fan TY, Xu K, Tsao SW, Wong YC. Activation of MAPK signaling pathway is essential for Id-1 induced serum independent prostate cancer cell growth. Oncogene 21: 8498-8505, 2002.
48. Liu L, Zhang X, Du C, Hou N, Zhao D, Sun J, Li L, Wang X, Ma C. MEK1-independent activation of MAPK and MEK1-dependent activation of p70 S6 kinase by stem cell factor (SCF) in ovarian cancer cells. Biochem Biophys Res Commun 382: 385-389, 2009.
49. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27: 441-464, 2011.
50. Maga G, Hubscher U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 116: 3051-3060, 2003.
51. Manso AM, Kang SM, Ross RS. Integrins, focal adhesions, and cardiac fibroblasts. J Investig Med 57: 856-860, 2009.
52. Marziliano N, Mannarino S, Nespoli L, Diegoli M, Pasotti M, Malattia C, Grasso M, Pilotto A, Porcu E, Raisaro A, Raineri C, Dore R, Maggio PP, Brega A, Arbustini E. Barth syndrome associated with compound hemizygosity and heterozygosity of the TAZ and LDB3 genes. Am J Med Genet A 143A: 907-915, 2007.
53. Matthiesen S, Bahulayan A, Holz O, Racke K. MAPK pathway mediates muscarinic receptor-induced human lung fibroblast proliferation. Life Sci 80: 2259-2262, 2007.
54. Mir SA, Chatterjee A, Mitra A, Pathak K, Mahata SK, Sarkar S. Inhibition of signal transducer and activator of transcription 3 (STAT3) attenuates interleukin-6 (IL-6)-induced collagen synthesis and resultant hypertrophy in rat heart. J Biol Chem 287: 2666-2677, 2012.
55. Naryzhny SN. Proliferating cell nuclear antigen: a proteomics view. Cell Mol Life Sci 65: 3789-3808, 2008.
56. Neustein HB, Lurie PR, Fugita M. Endocardial fibroelastosis found on transvascular endomyocardial biospsy in children. Arch Pathol Lab Med 103: 214-219, 1979.
57. Petrov VV, Fagard RH, Lijnen PJ. Stimulation of collagen production by transforming growth factor-beta1 during differentiation of cardiac fibroblasts to myofibroblasts. Hypertension 39: 258-263, 2002.
58. Phoon CKAD, Schlame M, Stocks DL, Edelman-Novemsky I, Yu D, Xu Y, Viswanathan N, Ren M. Tafazzin knockdown in mice leads to a developmental cardiomyopathy with early diastolic dysfunction preceding myocardial noncompaction. J Am Heart Assoc. In press.
59. Preeta R, Nair RR. Stimulation of cardiac fibroblast proliferation by cerium: a superoxide anion-mediated response. J Mol Cell Cardiol 31: 1573-1580, 1999.
60. Ravens U, Davia K, Davies CH, Gara P, Drake-Holland AJ, Hynd JW, Noble MI, Harding SE. Tachycardia-induced failure alters contractile properties of canine ventricular myocytes. Cardiovasc Res 32: 613-621, 1996.
61. Reynolds CM, Eguchi S, Frank GD, Motley ED. Signaling mechanisms of heparin-binding epidermal growth factor-like growth factor in vascular smooth muscle cells. Hypertension 39: 525-529, 2002.
62. Seo M, Kim Y, Lee YI, Kim SY, Ahn YM, Kang UG, Roh MS, Kim YS, Juhnn YS. Membrane depolarization stimulates the proliferation of SH-SY5Y human neuroblastoma cells by increasing retinoblastoma protein (RB) phosphorylation through the activation of cyclin-dependent kinase 2 (Cdk2). Neurosci Lett 404: 87-92, 2006.
63. Son Y, Cheong YK, Kim NH, Chung HT, Kang DG, Pae HO. Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J Signal Transduct 2011: 792639, 2011.
64. Spencer CT, Bryant RM, Day J, Gonzalez IL, Colan SD, Thompson WR, Berthy J, Redfearn SP, Byrne BJ. Cardiac and clinical phenotype in Barth syndrome. Pediatrics 118: e337-e346, 2006.
65. Stockand JD, Meszaros JG. Aldosterone stimulates proliferation of cardiac fibroblasts by activating Ki-RasA and MAPK1/2 signaling. Am J Physiol Heart Circ Physiol 284: H176-H184, 2003.
66. Sutherland RL, Watts CK, Musgrove EA. Cyclin gene expression and growth control in normal and neoplastic human breast epithelium. J Steroid Biochem Mol Biol 47: 99-106, 1993.
67. Tsutsui H, Kinugawa S, Matsushima S. Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol 301: H2181-H2190, 2011.
68. Valianpour F, Wanders RJ, Overmars H, Vreken P, Van Gennip AH, Baas F, Plecko B, Santer R, Becker K, Barth PG. Cardiolipin deficiency in X-linked cardioskeletal myopathy and neutropenia (Barth syndrome, MIM 302060): a study in cultured skin fibroblasts. J Pediatr 141: 729-733, 2002.
69. Vreken P, Valianpour F, Nijtmans LG, Grivell LA, Plecko B, Wanders RJ, Barth PG. Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem Biophys Res Commun 279: 378-382, 2000.
70. Wang M, Fang H, Han X. Shotgun lipidomics analysis of 4-hydroxyalkenal species directly from lipid extracts after one-step in situ derivatization. Anal Chem 84: 4580-4586, 2012.
71. Winer J, Jung CK, Shackel I, Williams PM. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270: 41-49, 1999.
72. Xu Y, Condell M, Plesken H, Edelman-Novemsky I, Ma J, Ren M, Schlame M. A Drosophila model of Barth syndrome. Proc Natl Acad Sci USA 103: 11584-11588, 2006.
73. Xu Y, Malhotra A, Ren M, Schlame M. The enzymatic function of tafazzin. J Biol Chem 281: 39217-39224, 2006.
74. Yang K, Cheng H, Gross RW, Han X. Automated lipid identification and quantification by multidimensional mass spectrometry-based shotgun lipidomics. Anal Chem 81: 4356-4368, 2009.
75. Yu HW, Liu QF, Liu GN. Positive regulation of the Egr-1/osteopontin positive feedback loop in rat vascular smooth muscle cells by TGF-beta, ERK, JNK, and p38 MAPK signaling. Biochem Biophys Res Commun 396: 451-456, 2010.
76. Zhu L. Tumour suppressor retinoblastoma protein Rb: a transcriptional regulator. Eur J Cancer 41: 2415-2427, 2005.
77. Zhu X, Ohtsubo M, Bohmer RM, Roberts JM, Assoian RK. Adhesiondependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein. J Cell Biol 133: 391-403, 1996.