Statin-triggered cell death in primary human lung mesenchymal cells involves p53-PUMA and release of Smac and Omi but not cytochrome c

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1803, Issue 4, 2010, Pages 452-467

  Ghavami, Saeid ^a,b   Mutawe, Mark M ^a,b   Hauff, Kristin ^a   Stelmack, Gerald L ^a,b   Schaafsma, Dedmer ^a,b   Sharma, Pawan ^a,b   McNeill, Karol D ^a,b   Hynes, Tyler S ^a,b   Kung, Sam K ^a   Unruh, Helmut ^a   Klonisch, Thomas ^a   Hatch, Grant M ^a   Los, Marek ^c   Halayko, Andrew J ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b MANITOBA INSTITUTE OF CHILD HEALTH   (Canada)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Airway smooth muscle; Apoptosis; Caspase; Fibroblast; Mitochondria; Statin

Indexed keywords

BH3 PROTEIN; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CHOLESTEROL; CYTOCHROME C; FARNESYL DIPHOSPHATE; GERANYLGERANYL PYROPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INHIBITOR OF APOPTOSIS PROTEIN; MEVALONIC ACID; MITOCHONDRIAL PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN DRP1; PROTEIN NOXA; PROTEIN P53; PUMA PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SIMVASTATIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ASTHMA; BREATHING MUSCLE; CELL DEATH; CHOLESTEROL SYNTHESIS; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EXPOSURE; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; LUNG FIBROBLAST; MESENCHYME CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CASPASE 8; CASPASE 9; CHOLESTEROL; CYTOCHROMES C; FIBROBLASTS; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG; MESODERM; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE, SMOOTH, VASCULAR; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; SIMVASTATIN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77950461308     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.12.005     Document Type: Article

References (73)

1. Goldstein J.L., Brown M.S. Regulation of the mevalonate pathway. Nature 1990, 343:425-430.
2. Liao J.K., Laufs U. Pleiotropic effects of statins. Annu. Rev. Pharmacol. Toxicol. 2005, 45:89-118.
3. Demierre M.F., Higgins P.D., Gruber S.B., Hawk E., Lippman S.M. Statins and cancer prevention. Nat. Rev. Cancer 2005, 5:930-942.
4. Wong W.W., Dimitroulakos J., Minden M.D., Penn L.Z. HMG-CoA reductase inhibitors and the malignant cell: the statin family of drugs as triggers of tumor-specific apoptosis. Leukemia 2002, 16:508-519.
5. Guijarro C., Blanco-Colio L.M., Ortego M., Alonso C., Ortiz A., Plaza J.J., Diaz C., Hernandez G., Egido J. 3-Hydroxy-3-methylglutaryl coenzyme a reductase and isoprenylation inhibitors induce apoptosis of vascular smooth muscle cells in culture. Circ. Res. 1998, 83:490-500.
6. Heusinger-Ribeiro J., Fischer B., Goppelt-Struebe M. Differential effects of simvastatin on mesangial cells. Kidney Int. 2004, 66:187-195.
7. Yokota K., Miyoshi F., Miyazaki T., Sato K., Yoshida Y., Asanuma Y., Akiyama Y., Mimura T. High concentration simvastatin induces apoptosis in fibroblast-like synoviocytes from patients with rheumatoid arthritis. J. Rheumatol. 2008, 35:193-200.
8. Wu J., Wong W.W., Khosravi F., Minden M.D., Penn L.Z. Blocking the Raf/MEK/ERK pathway sensitizes acute myelogenous leukemia cells to lovastatin-induced apoptosis. Cancer Res. 2004, 64:6461-6468.
9. Liao J.K. Isoprenoids as mediators of the biological effects of statins. J. Clin. Invest. 2002, 110:285-288.
10. Ghavami S., Hashemi M., Ande S.R., Yeganeh B., Xiao W., Eshraghi M., Bus C.J., Kadkhoda K., Wiechec E., Halayko A.J., Los M. Apoptosis and cancer: mutations within caspase genes. J. Med. Genet. 2009, 46:497-510.
11. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2002, 2:647-656.
12. Willis S.N., Chen L., Dewson G., Wei A., Naik E., Fletcher J.I., Adams J.M., Huang D.C. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 2005, 19:1294-1305.
13. Chipuk J.E., Bouchier-Hayes L., Kuwana T., Newmeyer D.D., Green D.R. PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 2005, 309:1732-1735.
14. Zong W.X., Lindsten T., Ross A.J., MacGregor G.R., Thompson C.B. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 2001, 15:1481-1486.
15. Thornberry N.A., Lazebnik Y. Caspases: enemies within. Science 1998, 281:1312-1316.
16. Ghavami S., Kerkhoff C., Chazin W.J., Kadkhoda K., Xiao W., Zuse A., Hashemi M., Eshraghi M., Schulze-Osthoff K., Klonisch T., Los M. S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochim. Biophys. Acta 2008, 1783:297-311.
17. Zou H., Li Y., Liu X., Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 1999, 274:11549-11556.
18. Shibata M.A., Ito Y., Morimoto J., Otsuki Y. Lovastatin inhibits tumor growth and lung metastasis in mouse mammary carcinoma model: a p53-independent mitochondrial-mediated apoptotic mechanism. Carcinogenesis 2004, 25:1887-1898.
19. Marcelli M., Cunningham G.R., Haidacher S.J., Padayatty S.J., Sturgis L., Kagan C., Denner L. Caspase-7 is activated during lovastatin-induced apoptosis of the prostate cancer cell line LNCaP. Cancer Res. 1998, 58:76-83.
20. Cafforio P., Dammacco F., Gernone A., Silvestris F. Statins activate the mitochondrial pathway of apoptosis in human lymphoblasts and myeloma cells. Carcinogenesis 2005, 26:883-891.
21. Elias J.A., Zhu Z., Chupp G., Homer R.J. Airway remodeling in asthma. J. Clin. Invest. 1999, 104:1001-1006.
22. Regamey N., Ochs M., Hilliard T.N., Muhlfeld C., Cornish N., Fleming L., Saglani S., Alton E.W., Bush A., Jeffery P.K., Davies J.C. Increased airway smooth muscle mass in children with asthma, cystic fibrosis, and non-cystic fibrosis bronchiectasis. Am. J. Respir. Crit. Care Med. 2008, 177:837-843.
23. Hothersall E., McSharry C., Thomson N.C. Potential therapeutic role for statins in respiratory disease. Thorax 2006, 61:729-734.
24. Ratjen F. New pulmonary therapies for cystic fibrosis. Curr. Opin. Pulm. Med. 2007, 13:541-546.
25. Zeki A.A., Franzi L., Last J., Kenyon N.J. Simvastatin inhibits airway hyperreactivity: implications for the mevalonate pathway and beyond. Am. J. Respir. Crit. Care Med. 2009, 180:731-740.
26. Gosens R., Stelmack G.L., Dueck G., McNeill K.D., Yamasaki A., Gerthoffer W.T., Unruh H., Gounni A.S., Zaagsma J., Halayko A.J. Role of caveolin-1 in p42/p44 MAP kinase activation and proliferation of human airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291:L523-L534.
27. Naureckas E.T., Ndukwu I.M., Halayko A.J., Maxwell C., Hershenson M.B., Solway J. Bronchoalveolar lavage fluid from asthmatic subjects is mitogenic for human airway smooth muscle. Am. J. Respir. Crit. Care Med. 1999, 160:2062-2066.
28. Ghavami S., Eshraghi M., Kadkhoda K., Mutawe M.M., Maddika S., Bay G.H., Wesselborg S., Halayko A.J., Klonisch T., Los M. Role of BNIP3 in TNF-induced cell death-TNF upregulates BNIP3 expression. Biochim. Biophys. Acta 2009, 1793:546-560.
29. Ghavami S., Asoodeh A., Klonisch T., Halayko A., Kadkhoda K., K.T., Gibson S.B., Booy E.P., Naderi-Manesh H., Los M. Brevinin-2R semi-selectively kills cancer cells by a distinct mechanism, which involves the lysosomal-mitochondrial death pathway. J. Cell. Mol. Med. 2008, 1-18.
30. Zhou M., Diwu Z., Panchuk-Voloshina N., Haugland R.P. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem. 1997, 253:162-168.
31. Mohanty J.G., Jaffe J.S., Schulman E.S., Raible D.G. A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. J. Immunol. Methods 1997, 202:133-141.
32. Mokashi V., Singh D.K., Porter T.D. Supernatant protein factor stimulates HMG-CoA reductase in cell culture and in vitro. Arch. Biochem. Biophys. 2005, 433:474-480.
33. Tang D., Park H.J., Georgescu S.P., Sebti S.M., Hamilton A.D., Galper J.B. Simvastatin potentiates tumor necrosis factor alpha-mediated apoptosis of human vascular endothelial cells via the inhibition of the geranylgeranylation of RhoA. Life Sci. 2006, 79:1484-1492.
34. Adrain C., Creagh E.M., Martin S.J. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J. 2001, 20:6627-6636.
35. Tran J., Kung S.K. Lentiviral vectors mediate stable and efficient gene delivery into primary murine natural killer cells. Mol. Ther. 2007, 15:1331-1339.
36. Sharma P., Tran T., Stelmack G.L., McNeill K., Gosens R., Mutawe M.M., Unruh H., Gerthoffer W.T., Halayko A.J. Expression of the dystrophin-glycoprotein complex is a marker for human airway smooth muscle phenotype maturation. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294:L57-L68.
37. van de Donk N.W., Kamphuis M.M., van Kessel B., Lokhorst H.M., Bloem A.C. Inhibition of protein geranylgeranylation induces apoptosis in myeloma plasma cells by reducing Mcl-1 protein levels. Blood 2003, 102:3354-3362.
38. Zhuang L., Kim J., Adam R.M., Solomon K.R., Freeman M.R. Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts. J. Clin. Invest. 2005, 115:959-968.
39. Gniadecki R. Depletion of membrane cholesterol causes ligand-independent activation of Fas and apoptosis. Biochem. Biophys. Res. Commun. 2004, 320:165-169.
40. Chipuk J.E., Kuwana T., Bouchier-Hayes L., Droin N.M., Newmeyer D.D., Schuler M., Green D.R. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303:1010-1014.
41. Maddika S., Ande S.R., Panigrahi S., Paranjothy T., Weglarczyk K., Zuse A., Eshraghi M., Manda K.D., Wiechec E., Los M. Cell survival, cell death and cell cycle pathways are interconnected: implications for cancer therapy. Drug Resist. Updat. 2007, 10:13-29.
42. Vousden K.H., Lu X. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2002, 2:594-604.
43. Komarov P.G., Komarova E.A., Kondratov R.V., Christov-Tselkov K., Coon J.S., Chernov M.V., Gudkov A.V. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999, 285:1733-1737.
44. Abdullaev Z., Bodrova M.E., Chernyak B.V., Dolgikh D.A., Kluck R.M., Pereverzev M.O., Arseniev A.S., Efremov R.G., Kirpichnikov M.P., Mokhova E.N., Newmeyer D.D., Roder H., Skulachev V.P. A cytochrome c mutant with high electron transfer and antioxidant activities but devoid of apoptogenic effect. Biochem J. 2002, 362:749-754.
45. Bilim V., Yuuki K., Itoi T., Muto A., Kato T., Nagaoka A., Motoyama T., Tomita Y. Double inhibition of XIAP and Bcl-2 axis is beneficial for retrieving sensitivity of renal cell cancer to apoptosis. Br. J. Cancer 2008, 98:941-949.
46. Tanaka A., Youle R.J. A chemical inhibitor of DRP1 uncouples mitochondrial fission and apoptosis. Mol. Cell 2008, 29:409-410.
47. Parone P.A., Martinou J.C. Mitochondrial fission and apoptosis: an ongoing trial. Biochim. Biophys. Acta 2006, 1763:522-530.
48. Parone P.A., James D.I., Da Cruz S., Mattenberger Y., Donze O., Barja F., Martinou J.C. Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol. Cell. Biol. 2006, 26:7397-7408.
49. James D.I., Parone P.A., Mattenberger Y., Martinou J.C. hFis1, a novel component of the mammalian mitochondrial fission machinery. J. Biol. Chem. 2003, 278:36373-36379.
50. Vaughan C.J., Murphy M.B., Buckley B.M. Statins do more than just lower cholesterol. Lancet 1996, 348:1079-1082.
51. Demyanets S., Kaun C., Pfaffenberger S., Hohensinner P.J., Rega G., Pammer J., Maurer G., Huber K., Wojta J. Hydroxymethylglutaryl-coenzyme A reductase inhibitors induce apoptosis in human cardiac myocytes in vitro. Biochem. Pharmacol. 2006, 71:1324-1330.
52. Connor A.M., Berger S., Narendran A., Keystone E.C. Inhibition of protein geranylgeranylation induces apoptosis in synovial fibroblasts. Arthritis Res. Ther. 2006, 8:R94.
53. Negre-Aminou P., van Vliet A.K., van Erck M., van Thiel G.C., van Leeuwen R.E., Cohen L.H. Inhibition of proliferation of human smooth muscle cells by various HMG-CoA reductase inhibitors; comparison with other human cell types. Biochim. Biophys. Acta 1997, 1345:259-268.
54. Stein O., Vanderhoek J., Friedman G., Stein Y. Deposition and mobilization of cholesterol ester in cultured human skin fibroblasts. Biochim. Biophys. Acta 1976, 450:367-378.
55. Diamant M., Tushuizen M.E., Abid-Hussein M.N., Hau C.M., Boing A.N., Sturk A., Nieuwland R. Simvastatin-induced endothelial cell detachment and microparticle release are prenylation dependent. Thromb. Haemost. 2008, 100:489-497.
56. Blanco-Colio L.M., Villa A., Ortego M., Hernandez-Presa M.A., Pascual A., Plaza J.J., Egido J. 3-Hydroxy-3-methyl-glutaryl coenzyme A reductase inhibitors, atorvastatin and simvastatin, induce apoptosis of vascular smooth muscle cells by downregulation of Bcl-2 expression and Rho A prenylation. Atherosclerosis 2002, 161:17-26.
57. Martindale J.L., Holbrook N.J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol. 2002, 192:1-15.
58. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., Liu J., Zhao X.D., Chew J.L., Lee Y.L., Kuznetsov V.A., Sung W.K., Miller L.D., Lim B., Liu E.T., Yu Q., Ng H.H., Ruan Y. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219.
59. Schuler M., Maurer U., Goldstein J.C., Breitenbucher F., Hoffarth S., Waterhouse N.J., Green D.R. p53 triggers apoptosis in oncogene-expressing fibroblasts by the induction of Noxa and mitochondrial Bax translocation. Cell Death Differ. 2003, 10:451-460.
60. Mashima T., Tsuruo T. Defects of the apoptotic pathway as therapeutic target against cancer. Drug Resist. Updat. 2005, 8:339-343.
61. Gross A., McDonnell J.M., Korsmeyer S.J. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 1999, 13:1899-1911.
62. Yu J., Zhang L., Hwang P.M., Kinzler K.W., Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell 2001, 7:673-682.
63. Shibue T., Takeda K., Oda E., Tanaka H., Murasawa H., Takaoka A., Morishita Y., Akira S., Taniguchi T., Tanaka N. Integral role of Noxa in p53-mediated apoptotic response. Genes Dev. 2003, 17:2233-2238.
64. Riedl S.J., Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell. Biol. 2004, 5:897-907.
65. Otera H., Ohsakaya S., Nagaura Z., Ishihara N., Mihara K. Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J. 2005, 24:1375-1386.
66. Arnoult D., Gaume B., Karbowski M., Sharpe J.C., Cecconi F., Youle R.J. Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J. 2003, 22:4385-4399.
67. van Loo G., van Gurp M., Depuydt B., Srinivasula S.M., Rodriguez I., Alnemri E.S., Gevaert K., Vandekerckhove J., Declercq W., Vandenabeele P. The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ. 2002, 9:20-26.
68. Bocan T.M. Pleiotropic effects of HMG-CoA reductase inhibitors. Curr. Opin. Investig. Drugs 2002, 3:1312-1317.
69. Laurent A., Nicco C., Chereau C., Goulvestre C., Alexandre J., Alves A., Levy E., Goldwasser F., Panis Y., Soubrane O., Weill B., Batteux F. Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer Res. 2005, 65:948-956.
70. Smirnova E., Shurland D.L., Ryazantsev S.N., van der Bliek A.M. A human dynamin-related protein controls the distribution of mitochondria. J. Cell. Biol. 1998, 143:351-358.
71. Ishihara N., Nomura M., Jofuku A., Kato H., Suzuki S.O., Masuda K., Otera H., Nakanishi Y., Nonaka I., Goto Y., Taguchi N., Morinaga H., Maeda M., Takayanagi R., Yokota S., Mihara K. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell. Biol. 2009, 11:958-966.
72. Maycotte P., Blancas S., Moran J. Role of inhibitor of apoptosis proteins and Smac/DIABLO in staurosporine-induced cerebellar granule neurons death. Neurochem. Res. 2008, 33:1534-1540.
73. Srinivasula S.M., Hegde R., Saleh A., Datta P., Shiozaki E., Chai J., Lee R.A., Robbins P.D., Fernandes-Alnemri T., Shi Y., Alnemri E.S. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001, 410:112-116.