ER stress activating ATF4/CHOP-TNF-α signaling pathway contributes to alcohol-induced disruption of osteogenic lineage of multipotential mesenchymal stem cell

Cellular Physiology and Biochemistry

Volumn 32, Issue 3, 2013, Pages 743-754

  Chen, Yueping ^a,b   Gao, Hui ^b   Yin, Qingshui ^c   Chen, Liang ^b   Dong, Panfeng ^b   Zhang, Xiaoyun ^b   Kang, Jie ^b  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b RUIKANG HOSPITAL AFFILIATED TO GUANGXI UNIVERSITY OF CHINESE MEDICINE   (China)

^c GUANGZHOU GENERAL HOSPITAL OF GUANGZHOU MILITARY COMMAND   (China)

Author keywords

Adipogenesis; ATF4; Bone marrow stem cells (BMSCs); CHOP; ER stress; Ethanol; Heat shock protein; Multipotential mesenchymal stem cells (MSC); Osteogenesis; Reactive oxygen species (ROS); TNF

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CASPASE 3; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; ALCOHOL; AP2 PROTEIN; FAT DROPLET; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ADULT; ALCOHOL CONSUMPTION; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL LINEAGE; CLINICAL ARTICLE; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LIPID STORAGE; MESENCHYMAL STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION; CELL DIFFERENTIATION; CONTROLLED STUDY; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; LONG TERM EXPOSURE; OSSIFICATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ACTIVATING TRANSCRIPTION FACTOR 4; ADIPOGENESIS; BONE MARROW CELLS; CASPASE 3; CELL LINEAGE; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; ETHANOL; FATTY ACID-BINDING PROTEINS; HEAT-SHOCK PROTEINS; HUMANS; MEMBRANE GLYCOPROTEINS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; PPAR GAMMA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84884997052     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000354476     Document Type: Article

References (41)

1. Włodarski KH: Haematopoietic and osteogenic bone marrow stem cells. Ortop Traumatol Rehabil 2011;13: 439-447.
2. Pignolo RJ, Shore EM: Circulating osteogenic precursor cells. Crit Rev Eukaryot Gene Expr 2010;20: 171-180.
3. Wu JY, Scadden DT, Kronenberg HM: Role of the osteoblast lineage in the bone marrow hematopoietic niches. J Bone Miner Res 2009;24: 759-764.
4. Heino TJ, Hentunen TA: Differentiation of osteoblasts and osteocytes from mesenchymal stem cells. Curr Stem Cell Res Ther 2008;3: 131-145.
5. Wahl EC, Aronson J, Liu L, Liu Z, Perrien DS, Skinner RA, Badger TM, Ronis MJ, Lumpkin CK Jr: Chronic ethanol exposure inhibits distraction osteogenesis in a mouse model: role of the TNF signaling axis. Toxicol Appl Pharmacol 2007;220: 302-310.
6. Wang Y, Li Y, Mao K, Li J, Cui Q, Wang GJ: Alcohol-induced adipogenesis in bone and marrow: a possible mechanism for osteonecrosis. Clin Orthop Relat Res 2003;410: 213-224.
7. Cui Q, Wang Y, Saleh KJ, Wang GJ, Balian G: Alcohol-induced adipogenesis in a cloned bone-marrow stem cell. J Bone Joint Surg Am 2006;88 Suppl 3: 148-154.
8. Rosa ML, Beloti MM, Prando N, Queiroz RH, de Oliveira PT, Rosa AL: Chronic ethanol intake inhibits in vitro osteogenesis induced by osteoblasts differentiated from stem cells. J Appl Toxicol 2008;28: 205-211.
9. Diamond T, Stiel D, Lunzer M, Wilkinson M, Posen S: Ethanol reduces bone formation and may cause osteoporosis. Am J Med 1989;86: 282-288.
10. Purohit V: Introduction to the alcohol and osteoporosis symposium. Alc Clin Exp Res 1997;21: 383-384.
11. Chen JR, Lazarenko OP, Shankar K, Blackburn ML, Badger TM, Ronis MJ: A role for ethanol-induced oxidative stress in controlling lineage commitment of mesenchymal stromal cells through inhibition of Wnt/beta-catenin signaling. J Bone Miner Res 2010;25: 1117-1127.
12. Nguyen KH, Lee JH, Nyomba BL: Ethanol causes endoplasmic reticulum stress and impairment of insulin secretion in pancreatic β-cells. Alcohol 2012;46: 89-99.
13. Nishitani Y, Matsumoto H: Ethanol rapidly causes activation of JNK associated with ER stress under inhibition of ADH. FEBS Lett 2006;580: 9-14.
14. Wek RC, Jiang HY, Anthony TG: Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 2006;34: 7-11.
15. Vattem KM, Wek RC: Reinitation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 2004;101: 11269-11274.
16. Saito A, Ochiai K, Kondo S, Tsumagari K, Murakami T, Cavener DR, Imaizumi K: Endoplasmic reticulum stress response mediated by the PERK-eIF2(alpha)-ATF4 pathway is involved in osteoblast differentiation induced by BMP2. J Biol Chem 2011;286: 4809-4818.
17. Karpinski BA, Morle GD, Huggenvik J, Uhler MD, Leiden JM: Molecular cloning of human CREB-2: an ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element. Proc Natl Acad Sci USA 1992;89: 4820-4824.
18. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP, Ron D: CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes & Development 2006;18: 3066-3077.
19. Oyadomari S, Mori M: Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004;11: 381-389.
20. Galehdar Z, Swan P, Fuerth B, Callaghan SM, Park DS, Cregan SP: Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J Neurosci 2010;30: 16938-16948.
21. Nishitoh H: CHOP is a multifunctional transcription factor in the ER stress response. J Biochem 2012;151: 217-219.
22. Hamamura K, Yokota H: Stress to endoplasmic reticulum of mouse osteoblasts induces apoptosis and transcriptional activation for bone remodeling. FEBS Lett 2007;581: 1769-1774.
23. Yang X, Matsuda K, Bialek P, Jacquot S, Masuoka HC, Schinke T, Li L, Brancorsini S, Sassone-Corsi P, Townes TM, Hanauer A, Karsenty G: ATF4 is a substrate of RSK2 and essential regulator of osteoblast biology: Implication for Coffin-Lowry Syndrome. Cell 2004;117: 387-398.
24. Komori T: Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 2006;99: 1233-1239.
25. Franceschi RT, Ge C, Xiao G, Roca H, Jiang D: Transcriptional regulation of osteoblasts. Ann N Y Acad Sci 2007;1116: 196-207.
26. Pereira RC, Stadmeyer LE, Smith DL, Rydziel S, Canalis E: CCAAT/Enhancer binding protein homologous protein (CHOP) decreases bone formation and causes osteopenia. Bone 2007;40: 619-626.
27. Shirakawa K, Maeda S, Gotoh T, Hayashi M, Shinomiya K, Ehata S, Nishimura R, Mori M, Onozaki K, Hayashi H, Uematsu S, Akira S, Ogata E, Miyazono K, Imamura T: CCAAT/Enhancer binding protein homologous protein (CHOP) regulates osteoblasts differentiation. Mol Cell Biol 2006;26: 6105-6116.
28. Kveiborg M, Sabatakos G, Chiusaroli R, Wu M, Philbrick WM, Horne WC, Baron R: DeltaFosB induces osteosclerosis and decreases adipogenesis by two independent cell-autonomous mechanisms. Mol Cell Biol 2004;24: 2820-2830.
29. Wahl EC, Perrien DS, Aronson J, Liu Z, Fletcher TW, Skinner RA, Feige U, Suva LJ, Badger TM, Lumpkin CK Jr: Ethanol-induced inhibition of bone formation in a rat model of distraction osteogenesis: a role for the tumor necrosis factor signaling axis. Alcohol Clin Exp Res 2005;29: 1466-1472.
30. Perrien DS, Liu Z, Wahl EC, Bunn RC, Skinner RA, Aronson J, Fowlkes J, Badger TM, Lumpkin CK Jr: Chronic ethanol exposure is associated with a local increase in TNF-alpha and decreased proliferation in the rat distraction gap. Cytokine 2003;23: 179-189.
31. Huang Q, Zhang H, Pei FX, Chen ZY, Wang GL, Shen B, Yang J, Zhou ZK, Kong QQ: Use of small interfering ribonucleic acids to inhibit the adipogenic effect of alcohol on human bone marrow-derived mesenchymal cells. Int Orthop 2010;34: 1059-1068.
32. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR: Multilineage potential of adult human mesenchymal stem cells. Science 1999;284: 143-147.
33. Klein RF: Alcohol-induced bone disease: impact of ethanol on osteoblast proliferation. Alcohol Clin Exp Res 1997;21: 392-399.
34. Komatsu S, Miyazawa K, Moriya S, Takase A, Naito M, Inazu M, Kohno N, Itoh M, Tomoda A: Clarithromycin enhances bortezomib-induced cytotoxicity via endoplasmic reticulum stress-mediated CHOP (GADD153) induction and autophagy in breast cancer cells. Int J Oncol 2012;40: 1029-1039.
35. Rzymski T, Milani M, Pike L, Buffa F, Mellor HR, Winchester L, Pires I, Hammond E, Ragoussis I, Harris AL: Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene 2010;29: 4424-4435
36. Liu ES, Lee AS: Common sets of nuclear factors binding to the conserved promoter sequence motif of two coordinately regulated ER protein genes, GRP78 and GRP94. Nucleic Acids Res 1991;19: 5425-5431.
37. Argon Y, Simen BB: GRP94, an ER chaperone with protein and peptide binding properties. Semin Cell Dev Biol 1999;10: 495-505.
38. Nanes MS: Tumor necrosis factor-α: molecular and cellular mechanisms in skeletal pathology. Gene 2003;321: 1-15.
39. Frost A, Jonsson K, Nilsson O, Ljunggren O: Inflammatory cytokines regulate proliferation of cultured human osteoblasts. Acta Ortho Scand 1997;68: 91-96.
40. Gerstenfeld L, Cho T, Kon T, Aizawa T, Cruceta J, Graves B, Einhorn T: Impaired intramembranous bone formation during bone repair in the absence of tumor necrosis factor-alpha signaling. Cells Tissues Organs 2001;169: 285-294.
41. Perrien DS, Brown EC, Fletcher TW, Irby DJ, Aronson J, Gao GG, Skinner RA, Hogue WR, Feige U, Suva LJ, Ronis MJ, Badger TM, Lumpkin CK Jr: Interleukin-1 and tumor necrosis factor antagonists attenuate ethanol-induced inhibition of bone formation in a rat model of distraction osteogenesis. J Pharmacol Exp Ther 2002;303: 904-908.