Effects of nicotine on proliferation and osteoblast differentiation in human alveolar bone marrow-derived mesenchymal stem cells
Abstract
Aims Nicotine is a risk factor for various diseases, including osteoporosis, oral cancer, and periodontal disease. Numerous studies have elucidated the effects of nicotine on cell proliferation and differentiation. The purpose of this study was to determine the effects of nicotine on the proliferation and osteoblast differentiation of human alveolar bone marrow-derived mesenchymal stem cells (hABMMSCs).Main methods In this study, we treated hABMMSCs with different doses (1 μM to 5 mM) of nicotine. The survival and proliferation of hABMMSCs were evaluated by the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium (MTT) assay and crystal violet assay. TUNEL and propidium iodide (PI) double staining assay were also performed. The effect of nicotine on osteoblast differentiation of hABMMSCs was determined by measuring calcium accumulation using alizarin red-sulfate (AR-S) staining, measurement of alkaline phosphatase (ALP) activity, and semi-quantitative PCR of osteoblast markers.Key findings The survival and proliferation of hABMMSCs did not differ when they were exposed to nicotine at concentrations ranging from 1 μM to 100 μM; however, cell proliferation increased when the cells were exposed to nicotine at concentrations of 1-2 mM and decreased significantly when exposed to 5mM of nicotine. A number of cells were stained by PI but not by TUNEL, and membrane vacuolization was observed in hABMMSCs treated with 5mM nicotine. Calcium accumulation; ALP activity; and mRNA levels of ALP, bone sialoprotein (BSP), collagen type I α 1 (Col1αI), and runt-related transcription factor 2 (Runx2) were significantly decreased by treatment with 2mM of nicotine, while osteocalcin transcripts decreased by treatment with 1 to 2 mM of nicotine.Significance These results suggest that nicotine has a bimodal effect on the proliferation and osteoblast differentiation in hABMMSCs.
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Smoking exerts a direct effect on bone tissue via nicotinic acetylcholine receptors on osteoblasts, and nicotine's effect is dose-dependent: low concentrations stimulate osteoblast proliferation, whereas higher concentrations inhibit it.
“Based on the findings of Kim and colleagues, the effect is dose-dependent—at low concentrations, nicotine appears to have a stimulating effect on osteoblast proliferation, whereas at higher concentrations, the effect is inhibitory [43].”
From Skeletal System Biology and Smoke Damage: From Basic Science to Medical Clinic (2021) · cites this paper as [43]
Cites
Pharmacologic Aspects of Cigarette Smoking and Nicotine Addiction
Oates, J. A., Wood, A. J. J., & Benowitz, N. L. (1988) · New England Journal of Medicine · doi:10.1056/nejm198811173192005 · Cited by 963 · see citing works
Lee, K., Kim, H., Li, Q., Chi, X., Ueta, C., Komori, T., Wozney, J. M., Kim, E., Choi, J.-Y., Ryoo, H., et al. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.23.8783-8792.2000 · Cited by 867 · see citing works
Self-citationExpression of differentiated function by mineralizing cultures of chicken osteoblasts
Gerstenfeld, L. C., Chipman, S. D., Glowacki, J., & Lian, J. B. (1987) · Developmental Biology · doi:10.1016/0012-1606(87)90331-9 · Cited by 397 · see citing works
Matsubara, T., Suardita, K., Ishii, M., Sugiyama, M., Igarashi, A., Oda, R., Nishimura, M., Saito, M., Nakagawa, K., Yamanaka, K., et al. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.041117 · Cited by 322 · see citing works
Wang, X., Kua, H.-Y., Hu, Y., Guo, K., Zeng, Q., Wu, Q., Ng, H., Karsenty, G., Crombrugghe, B. D., Yeh, J. K., et al. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200507106 · Cited by 250 · see citing works
Disruption of thetalin gene arrests mouse development at the gastrulation stage
Monkley, S. J., Zhou, X.-H., Kinston, S., Giblett, S. M., Hemmings, L., Priddle, H., Brown, J., Pritchard, C. A., Critchley, D. R., & F�ssler, R. (2000) · Developmental Dynamics · doi:10.1002/1097-0177(2000)9999:9999 · Cited by 218 · see citing works
Effects of nicotine on cellular function in UMR 106-01 osteoblast-like cells☆
Fang, M. A., Frost, P., Iida‐Klein, A., & Hahn, T. J. (1991) · Bone · doi:10.1016/8756-3282(91)90077-v · Cited by 207 · see citing works
Oral tissue alterations associated with the use of smokeless tobacco by teen-agers
Greer, R. O., & Poulson, T. C. (1983) · Oral Surgery Oral Medicine Oral Pathology · doi:10.1016/0030-4220(83)90009-9 · Cited by 182 · see citing works
Thirunavukkarasu, K., Halladay, D., Miles, R. R., Yang, X., Galvin, R. J. S., Chandrasekhar, S., Martin, T. J., & Onyia, J. E. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000322200 · Cited by 181 · see citing works
Nicotine modulates bone metabolism-associated gene expression in osteoblast cells
Rothem, D. E., Rothem, L., Soudry, M., Dahan, A., & Eliakim, R. (2009) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-009-0075-5 · Cited by 167 · see citing works
Ramp, W. K., Lenz, L. G., & Galvin, R. J. S. (1991) · Experimental Biology and Medicine · doi:10.3181/00379727-197-43221 · Cited by 135 · see citing works
Cigarette Smoke Prevents Apoptosis through Inhibition of Caspase Activation and Induces Necrosis
Wickenden, J. A., Clarke, M. C. H., Rossi, A. G., Rahman, I., Faux, S. P., Donaldson, K., & MacNee, W. (2003) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2002-0235oc · Cited by 132 · see citing works
Raulin, L. A., McPherson, J. C., McQuade, M. J., & Hanson, B. S. (1988) · Journal of Periodontology · doi:10.1902/jop.1988.59.5.318 · Cited by 130 · see citing works
Influence of smoking on osseointegrated implant failure: a meta‐analysis
Hinode, D., Tanabe, S., Yokoyama, M., Fujisawa, K., Yamauchi, E., & Miyamoto, Y. (2006) · Clinical Oral Implants Research · doi:10.1111/j.1600-0501.2005.01244.x · Cited by 126 · see citing works
Cigarette Smoke Extract Induces DNA Damage but Not Apoptosis in Human Bronchial Epithelial Cells
Liu, X., Conner, H., Kobayashi, T., Kim, H., Wen, F., Abe, S., Fang, Q., Wang, X., Hashimoto, M., Bitterman, P. B., et al. (2005) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2003-0341oc · Cited by 112 · see citing works
Self-citationBinding, Uptake, and Release of Nicotine by Human Gingival Fibroblasts
Hanes, P. J., Schuster, G. S., & Lubas, S. (1991) · Journal of Periodontology · doi:10.1902/jop.1991.62.2.147 · Cited by 110 · see citing works
Chondrogenic cell differentiation from membrane bone periostea
Fang, J., & Hall, B. K. (1997) · Anatomy and Embryology · doi:10.1007/s004290050104 · Cited by 93 · see citing works
Zhou, X., Sheng, Y., Yang, R., & Kong, X. (2010) · The Cardiology · doi:10.1159/000301278 · Cited by 82 · see citing works
Bolin, A., Lavstedt, S., Frithiof, L., & Henrikson, C. O. (1986) · Acta Odontologica Scandinavica · doi:10.3109/00016358609004732 · Cited by 76 · see citing works
Osteoactivin acts as downstream mediator of BMP‐2 effects on osteoblast function
Abdelmagid, S. M., Barbe, M. F., Arango‐Hisijara, I., Owen, T. A., Popoff, S. N., & Safadi, F. F. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20841 · Cited by 76 · see citing works
Nicotine-induced alterations in human primary periodontal ligament and gingiva fibroblast cultures
Alpar, B., Leyhausen, G., Sapotnick, A., Günay, H., & Geurtsen, W. (1998) · Clinical Oral Investigations · doi:10.1007/s007840050042 · Cited by 57 · see citing works
Nicotine affects mineralized nodule formation by the human osteosarcoma cell line Saos-2
Tanaka, H., Tanabe, N., Suzuki, N., Shoji, M., Torigoe, H., Sugaya, A., Motohashi, M., & Maeno, M. (2005) · Life Sciences · doi:10.1016/j.lfs.2005.02.022 · Cited by 55 · see citing works
Giannopoulou, C., Roehrich, N., & Mombelli, A. (2001) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2001.280808.x · Cited by 55 · see citing works
Effects of nicotine on gene expression and osseointegration in rats
Yamano, S., Berley, J. A., Kuo, W. P., Gallucci, G. O., Weber, H., & Sukotjo, C. (2010) · Clinical Oral Implants Research · doi:10.1111/j.1600-0501.2010.01955.x · Cited by 55 · see citing works
Kim, B., Yoon-Chul, K. I. M., Zadeh, H. H., Park, Y., Pi, S., Shin, H., & You, H. (2011) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.100379 · Cited by 48 · see citing works
Self-citationSato, T., Abe, T., Nakamoto, N., Tomaru, Y., Koshikiya, N., Nojima, J., Kokabu, S., Sakata, Y., Kobayashi, A., & Yoda, T. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.09.114 · Cited by 45 · see citing works
Tobacco smoking and periodontal diseases.
Qandil, R., Sandhu, H. S., & Matthews, D. (1997) · PubMed · Cited by 44 · see citing works
Nicotine suppresses bone sialoprotein gene expression
Nakayama, Y., Mezawa, M., Araki, S., Sasaki, Y., Wang, S., Han, J., Li, X., Takai, H., & Ogata, Y. (2008) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2008.01171.x · Cited by 26 · see citing works
Suppressive effects of nicotine on the cytodifferentiation of murine periodontal ligament cells
Yanagita, M., Kojima, Y., Kawahara, T., Kajikawa, T., Oohara, H., Takedachi, M., Yamada, S., & Murakami, S. (2010) · Oral Diseases · doi:10.1111/j.1601-0825.2010.01693.x · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Use of Mesenchymal Stem Cells for Therapy of Cardiac Disease
Karantalis, V., & Hare, J. M. (2015) · Circulation Research · doi:10.1161/circresaha.116.303614 · Cited by 429 · see citing works
Liu, J., Yu, F., Sun, Y., Jiang, B., Zhang, W., Yang, J., Xu, G., Liang, A., & Liu, S. (2014) · Stem Cells · doi:10.1002/stem.1909 · Cited by 361 · see citing works
Therapeutic potential of dental stem cells
Chalisserry, E. P., Nam, S. Y., Park, S. H., & Anil, S. (2017) · Journal of Tissue Engineering · doi:10.1177/2041731417702531 · Cited by 209 · see citing works
Cigarette smoking and musculoskeletal disorders
Abate, M. (2013) · Muscles Ligaments and Tendons Journal · doi:10.11138/mltj/2013.3.2.063 · Cited by 158 · see citing works
Ebersole, J. L., Samburova, V., Son, Y., Cappelli, D. P., Demopoulos, C. A., Capurro, A., Pinto, A., Chrzan, B., Kingsley, K., Howard, K. M., et al. (2020) · Tobacco Induced Diseases · doi:10.18332/tid/116988 · Cited by 132 · see citing works
Cigarette smoking and musculoskeletal disorders
Abate, M., Vanni, D., Pantalone, A., & Salini, V. (2019) · Muscle Ligaments and Tendons Journal · doi:10.32098/mltj.02.2013.03 · Cited by 111 · see citing works
Emerging factors affecting peri‐implant bone metabolism
Ínsua, Á., Galindo‐Moreno, P., Miron, R. J., Wang, H., & Monje, A. (2023) · Periodontology 2000 · doi:10.1111/prd.12532 · Cited by 114 · see citing works
Xie, C., Du, L., Guo, F., Li, X., & Cheng, B. (2019) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-019-03526-7 · Cited by 107 · see citing works
Marinucci, L., Balloni, S., Fettucciari, K., Bodo, M., Talesa, V. N., & Antognelli, C. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.01.017 · Cited by 101 · see citing works
Aspera-Werz, R. H., Ehnert, S., Heid, D., Zhu, S., Chen, T., Braun, B., Sreekumar, V., Arnscheidt, C., & Nussler, A. K. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/3172480 · Cited by 90 · see citing works
Potential mechanisms linking psychological stress to bone health
Ng, J.-S., & Chin, K.-Y. (2021) · International Journal of Medical Sciences · doi:10.7150/ijms.50680 · Cited by 66 · see citing works
An Overlooked Bone Metabolic Disorder: Cigarette Smoking-Induced Osteoporosis
Weng, W., Li, H., & Zhu, S. (2022) · Genes · doi:10.3390/genes13050806 · Cited by 65 · see citing works
Nicotine Alters MicroRNA Expression and Hinders Human Adult Stem Cell Regenerative Potential
Ng, T. K., Carballosa, C. M., Pelaez, D., Wong, H. K., Choy, K. W., Pang, C. P., & Cheung, H. S. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0434 · Cited by 64 · see citing works
Wang, J., Liao, L., Wang, S., & Tan, M. J. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.01.218 · Cited by 63 · see citing works
Thein vitroandin vivoeffects of nicotine on bone, bone cells and fracture repair
Kallala, R., Barrow, J., Graham, S. M., Kanakaris, N. K., & Giannoudis, P. V. (2013) · Expert Opinion on Drug Safety · doi:10.1517/14740338.2013.770471 · Cited by 63 · see citing works
Skeletal System Biology and Smoke Damage: From Basic Science to Medical Clinic
Tarantino, U., Cariati, I., Greggi, C., Gasbarra, E., Belluati, A., Ciolli, L., Maccauro, G., Momoli, A., Ripanti, S., Falez, F., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126629 · Cited by 52 · see citing works
Li, Y., Chen, Y., Shen, G., Li, G., Shen, J., Xu, Y., & Gong, J. (2015) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmv013 · Cited by 43 · see citing works
Daffner, S. D., Waugh, S., Norman, T. L., Mukherjee, N., & France, J. C. (2012) · Global Spine Journal · doi:10.1055/s-0032-1326946 · Cited by 40 · see citing works
Association Between Prenatal Exposure to Alcohol and Tobacco and Neonatal Brain Activity
Shuffrey, L. C., Myers, M. M., Isler, J. R., Lucchini, M., Sania, A., Pini, N., Nugent, J. D., Condon, C. G., Ochoa, T. N., Brink, L. T., et al. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.4714 · Cited by 38 · see citing works
Greenberg, J. M., Carballosa, C. M., & Cheung, H. S. (2017) · Stem Cells Translational Medicine · doi:10.1002/sctm.17-0060 · Cited by 37 · see citing works
Sreekumar, V., Aspera-Werz, R. H., Ehnert, S., Strobel, J., Tendulkar, G., Heid, D., Schreiner, A. J., Arnscheidt, C., & Nussler, A. K. (2017) · Archives of Toxicology · doi:10.1007/s00204-017-2149-9 · Cited by 37 · see citing works
Marinucci, L., Bodo, M., Balloni, S., Locci, P., & Baroni, T. (2014) · Journal of Cellular Physiology · doi:10.1002/jcp.24661 · Cited by 36 · see citing works
Quantitative analyses of bone composition in acetylcholine receptor M3R and alpha7 knockout mice
Kliemann, K. R., Kneffel, M., Bergen, I., Kampschulte, M., Langheinrich, A. C., Dürselen, L., Ignatius, A. A., Kilián, O., Schnettler, R., & Lips, K. S. (2012) · Life Sciences · doi:10.1016/j.lfs.2012.07.024 · Cited by 35 · see citing works
Yue, C., Cui, G., Ma, M., Tang, Y., Li, H., Liu, Y., & Zhang, X. (2022) · Frontiers in Surgery · doi:10.3389/fsurg.2022.970537 · Cited by 34 · see citing works
Xie, G., Huang, C., Jiang, S., Li, H., Gao, Y., Zhang, T., Zhang, Q., Pavel, V., Rahmati, M., & Li, Y. (2024) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2024.04.003 · Cited by 33 · see citing works
Otero, C. E., Noeker, J. A., Brown, M. M., Wavreil, F. D. M., Harvey, W. A., Mitchell, K. A., & Heggland, S. J. (2019) · Journal of Applied Toxicology · doi:10.1002/jat.3777 · Cited by 33 · see citing works
The Role of Tocotrienol in Preventing Male Osteoporosis—A Review of Current Evidence
Chin, K., & Ima-Nirwana, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20061355 · Cited by 33 · see citing works
Calabrese, E. J. (2021) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2021.109730 · Cited by 33 · see citing works
Shen, Y. L., Liu, H., Ying, X., Yang, S., Nie, P., Cheng, S., Wang, W., Cheng, X., Peng, L., & Xu, H. (2013) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24512 · Cited by 31 · see citing works
Hormesis and embryonic stem cells
Calabrese, E. J. (2021) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2021.109783 · Cited by 29 · see citing works
Kim, D. H., Liu, J., Bhat, S., Benedict, G. M., Lecka‐Czernik, B., Peterson, S. J., Ebraheim, N. A., & Heck, B. E. (2012) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-012-0382-0 · Cited by 28 · see citing works
Efficacy of vitamins E and C for reversing the cytotoxic effects of nicotine and cotinine
Torshabi, M., Esfahrood, Z. R., Jamshidi, M., Torshizi, A. M., & Sotoudeh, S. (2017) · European Journal Of Oral Sciences · doi:10.1111/eos.12375 · Cited by 26 · see citing works
Nicotine inhibits MAPK signaling and spheroid invasion in ovarian cancer cells
Harmych, S. J., Kumar, J. P., Bouni, M. E., & Chadee, D. N. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112167 · Cited by 25 · see citing works
Effects of Palm Vitamin E on Bone-Formation-Related Gene Expression in Nicotine-Treated Rats
Abukhadir, S. S. A., Mohamed, N., Makpol, S., & Muhammad, N. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/656025 · Cited by 25 · see citing works
Aspera-Werz, R. H., Ehnert, S., Müller, M., Zhu, S., Chen, T., Weng, W., Jacoby, J., & Nussler, A. K. (2020) · World Journal of Stem Cells · doi:10.4252/wjsc.v12.i8.841 · Cited by 24 · see citing works
Gualberto, E. C., Theodoro, L. H., Longo, M., Novaes, V. C. N., Nagata, M. J. H., Ervolino, E., & Garcia, V. G. (2015) · Lasers in Medical Science · doi:10.1007/s10103-015-1820-8 · Cited by 24 · see citing works
Li, T., Zhang, J., Zhang, N., Zhang, N., Zeng, Y., Tang, S., Tao, Z., Qu, X., Jia, J., Zhu, W., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.22712 · Cited by 24 · see citing works
The effect of nicotine and cotinine on human gingival fibroblasts attachment to root surfaces
Esfahrood, Z. R., Zamanian, A., Torshabi, M., & Abrishami, M. (2015) · Journal of Basic and Clinical Physiology and Pharmacology · doi:10.1515/jbcpp-2014-0120 · Cited by 23 · see citing works
Kauschke, V., Gebert, A., Calin, M., Eckert, J., Scheich, S., Heiß, C., & Lips, K. S. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193468 · Cited by 23 · see citing works
Gao, S., Cheng, L. J., Li, K., Liu, W.-H., Xu, M., Jiang, W. H., Wei, L., Zhang, F., Xiao, W., Xiong, Y., et al. (2012) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-13-105 · Cited by 21 · see citing works
Dusabineza, A.-C., Najimi, M., Hul, N. V., Legry, V., Khuu, D. N., van Grunsven, L. A., Sokal, E. M., & Leclercq, I. A. (2015) · Cell Transplantation · doi:10.3727/096368915x686788 · Cited by 21 · see citing works
Low-dose nicotine reduces the homing ability of murine BMSCs during fracture healing.
Zhang, J., Wan, Q., Yu, X., Cheng, G., Ni, Y., & Li, Z. (2018) · Europe PMC (PubMed Central) · Cited by 18 · see citing works
Qu, Q., Zhang, F., Zhang, X., & Yin, W. (2017) · Dose-Response · doi:10.1177/1559325817739760 · Cited by 17 · see citing works
Comparison of the effect of cigarette smoke on mesenchymal stem cells and dental stem cells
Nguyen, B. T., Alpagot, T., Oh, H., Ojcius, D. M., & Xiao, N. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00217.2020 · Cited by 16 · see citing works
Zhong, Z.-G., Li, Y., Chen, Y., Chen, W., Li, S., Lv, X., & Luo, S. (2021) · Drug Design Development and Therapy · doi:10.2147/dddt.s293455 · Cited by 16 · see citing works
Gruber, M. D., Gibbs, D. L., Vignolles‐Jeong, J., Viljoen, S., Grossbach, A. J., & Xu, D. S. (2023) · Neurosurgery · doi:10.1227/neu.0000000000002412 · Cited by 16 · see citing works
Effects of nicotine on bone during orthodontic tooth movement in male rats
Bakathir, M. A., Linjawi, A. I., Omar, S. S., Aboqura, A. B., & Hassan, A. H. (2016) · Saudi Medical Journal · doi:10.15537/smj.2016.10.15159 · Cited by 16 · see citing works
Heikkinen, J., Tanner, T., Bergmann, U., Palosaari, S., & Lehenkari, P. P. (2024) · Tobacco Induced Diseases · doi:10.18332/tid/185281 · Cited by 15 · see citing works
Zhu, Y., Koleck, T. A., Bender, C. M., & Conley, Y. P. (2019) · Biological Research For Nursing · doi:10.1177/1099800419895114 · Cited by 14 · see citing works
Spatial Distributions, Characteristics, and Applications of Craniofacial Stem Cells
Zhang, G., Li, Q., Yuan, Q., & Zhang, S. (2020) · Stem Cells International · doi:10.1155/2020/8868593 · Cited by 14 · see citing works
de Almeida, J. M., de Moraes, R. O., Gusman, D. J. R., Faleiros, P. L., Nagata, M. J. H., Garcia, V. G., Theodoro, L. H., & Bosco, Á. F. (2016) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2016.12.003 · Cited by 14 · see citing works
Tobacco heating system has less impact on bone metabolism than cigarette smoke
Weng, W., Bovard, D., Zanetti, F., Ehnert, S., Braun, B., Uynuk‐Ool, T., Histing, T., Hoeng, J., Nussler, A. K., & Aspera-Werz, R. H. (2023) · Food and Chemical Toxicology · doi:10.1016/j.fct.2023.113637 · Cited by 13 · see citing works
Role of SIRT3 in bone homeostasis and its application in preventing and treating bone diseases
Xu, K., Li, J., Wen, R., Chang, B., Cheng, Y., & Yi, X. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1248507 · Cited by 13 · see citing works
Sung, I., Park, B.-C., Hah, Y., Cho, H. Y., Yun, J., Park, B.-W., Kang, Y., Kim, H., Hwang, S., Rho, G., et al. (2015) · International Journal of Medical Sciences · doi:10.7150/ijms.13172 · Cited by 12 · see citing works
Self-citationKamel, A. H. M., Kamal, S. M., & AbuBakr, N. (2020) · Dental and Medical Problems · doi:10.17219/dmp/113179 · Cited by 12 · see citing works
Limlawan, P., & Vacharaksa, A. (2025) · Frontiers in Oral Health · doi:10.3389/froh.2025.1423226 · Cited by 9 · see citing works
The effects of cigarette smoking and nicotine on the therapeutic potential of mesenchymal stem cells
Harrell, C. R., Djonov, V., & Volarević, V. (2022) · Hispana · doi:10.14670/hh-18-400 · Cited by 9 · see citing works
Torshabi, M., Esfahrood, Z. R., Gholamin, P., & Karami, E. (2016) · Journal of Basic and Clinical Physiology and Pharmacology · doi:10.1515/jbcpp-2015-0143 · Cited by 8 · see citing works
Boric Acid Reverses Nicotine-Induced Cytokine Expressions of Human Gingival Fibroblasts
Bozkurt, Ş. B., Nielsen, F. H., & Hakki, S. S. (2022) · Biological Trace Element Research · doi:10.1007/s12011-022-03243-1 · Cited by 7 · see citing works
Milovanovic, P. D., Stojanović, M., Antonijević, D., Ćirović, A., Radenković, M., & Djuric, M. P. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.09.044 · Cited by 7 · see citing works
Park, S.-R., Kim, S., Kim, S., Yu, W., Lee, S., & Lee, H.-Y. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03061-1 · Cited by 7 · see citing works
Self-citationAcute exposure to electronic cigarette components alters mRNA expression of pre‐osteoblasts
Dabdoub, S. M., Greenlee, A. N., Abboud, G., Brengartner, L., Zuiker, E., Gorr, M. W., Wold, L. E., Kumar, P., & Cray, J. (2024) · The FASEB Journal · doi:10.1096/fj.202302014rrr · Cited by 6 · see citing works
Harrell, C. R., Djonov, V., & Volarević, V. (2022) · PubMed · doi:10.48350/161873 · Cited by 6 · see citing works
The associations of implant and patient factors with migration of the tibial component differ by sex
Laende, E. K., Flemming, J. M., Wilson, J. L. A., Cantoni, E., & Dunbar, M. (2022) · The Bone & Joint Journal · doi:10.1302/0301-620x.104b4.bjj-2021-1247.r1 · Cited by 5 · see citing works
Fang, J., Wang, D., Yang, H.-Y., Zhang, H., Tong, J., & Lin, Z. (2022) · International Journal of Endocrinology · doi:10.1155/2022/6830705 · Cited by 5 · see citing works
Nilawati, N., Widyastuti, W., Rizka, Y., & Kurniawan, H. (2022) · European Journal of Dentistry · doi:10.1055/s-0042-1758794 · Cited by 5 · see citing works
Bozkurt, Ş. B., & Hakki, S. S. (2019) · Journal of Periodontology · doi:10.1002/jper.19-0256 · Cited by 5 · see citing works
Miah, M. L., Hossain, M. F., Uddin, M. E., Rahman, M. H., Barua, H., Osman, A. A., Khan, M. Z. H., & Sheikh, M. R. (2024) · Bioresearch Communications · doi:10.3329/brc.v11i1.78881 · Cited by 4 · see citing works
Ohno, Y., Taura, D., Okamoto, K., Fujita, H., Honda-Kohmo, K., Matsuo, K., & Sone, M. (2023) · Stem Cells and Development · doi:10.1089/scd.2022.0258 · Cited by 4 · see citing works
Bao, S., Jimu, W., Mu, N., Yan, F., Xing, S., & Zhou, Z. (2024) · Tobacco Induced Diseases · doi:10.18332/tid/194680 · Cited by 3 · see citing works
Nosrati, S., Gheisari, M., Zare, S., Dara, M., Zolghadri, S., & Razeghian‐Jahromi, I. (2024) · Tissue and Cell · doi:10.1016/j.tice.2024.102361 · Cited by 3 · see citing works
Sari, R. P., & Kurniawan, H. (2019) · Dental Journal (Majalah Kedokteran Gigi) · doi:10.20473/j.djmkg.v52.i4.p177-182 · Cited by 3 · see citing works
MicroRNA Signatures in Dental Pulp Stem Cells Following Nicotine Exposure
Vang, D., Hardin, L. T., Abid, N., Thor, D., & Xiao, N. (2025) · Dentistry Journal · doi:10.3390/dj13080338 · Cited by 2 · see citing works
Gheisari, M., Nosrati, S., Zare, S., Dara, M., Zolghadri, S., & Razeghian‐Jahromi, I. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1323691 · Cited by 2 · see citing works
Esfahrood, Z. R., Sarlak, H., Torshabi, M., Hartoonian, S., & Shekarchi, F. (2025) · BMC Oral Health · doi:10.1186/s12903-025-06386-4 · Cited by 2 · see citing works
Morsy, R. A. A., Sarhan, S. M., Rashed, L. A., Attia-Zoua, M. G., Ahmed, M. M., El-Batran, M. M., & Soliman, N. L. (2018) · Journal of Biological Sciences · doi:10.3923/jbs.2018.107.114 · Cited by 2 · see citing works
Recent Advances in Stem Cells for Dental Tissue Engineering
Nizami, M. Z. I., & Nishina, Y. (2021) · Springer eBooks · doi:10.1007/978-981-16-4420-7_12 · Cited by 2 · see citing works
Tao, X., Li, H., Xing, Y., Liu, F., Hu, Y., Tao, H., Mu, M., Pang, G., & Zhang, R. (2019) · Indian Journal of Pharmaceutical Sciences · doi:10.36468/pharmaceutical-sciences.597 · Cited by 2 · see citing works
Tamai, K., Formanek, B. G., Chamnan, R., Wang, J. C., & Buser, Z. (2020) · The Spine Journal · doi:10.1016/j.spinee.2019.09.016 · Cited by 2 · see citing works
Impact of cigarette smoke on the functions of mesenchymal stem cells
Pavlovic, D., Papic, D., Nićiforović, D., & Volarević, V. (2025) · Cell Transplantation · doi:10.1177/09636897251374178 · Cited by 1 · see citing works
Stem Cells from Human Dental Tissue for Regenerative Medicine
Liu, J., & Liu, S. (2016) · doi:10.1002/9781119135449.ch24 · Cited by 1 · see citing works
Skeletal age estimation and the epiphyseal scar : challenging the status quo
Davies, C. M. (2013)
Madrid, J. V. (2018) · CSUSB ScholarWorks (California State University, San Bernardino)
The effect of smoking on stem cell mobilization in allogeneic donors
Yiğenoğlu, T. N., Başçı, S., Şahin, D., Bakırtaş, M., Kılınç, A., Ulu, B. U., Batgi, H., İskender, D., Özcan, N., Çakar, M. K., et al. (2020) · Journal of Health Sciences and Medicine · doi:10.32322/jhsm.729505
Park, S.-R., Kim, S., Kim, S., & Lee, H.-Y. (2022) · Research Square · doi:10.21203/rs.3.rs-1483706/v1
Self-citationBorik Asitin Sementoblast Hücrelerinde Nikotin Kaynaklı Biyoaktivite Kaybı Üzerindeki Etkisi
ÜNLÜTÜRK, M., HASIRCI, A. E., & Bozkurt, Ş. B. (2023) · Journal of Boron · doi:10.30728/boron.1316579
Herbst, M., Aspera-Werz, R. H., Braun, B. J., Schulz, K., Rollmann, M. F. R., Histing, T., & Nussler, A. K. (2024) · Research Square · doi:10.21203/rs.3.rs-4241378/v1
Herbst, M., Aspera-Werz, R. H., Braun, B. J., Schulz, K., Rollmann, M. F. R., Histing, T., & Nussler, A. K. (2024) · Qeios · doi:10.32388/de0eae
Herbst, M., Aspera-Werz, R. H., Braun, B. J., Schulz, K., Rollmann, M. F. R., Histing, T., & Nussler, A. K. (2024) · Qeios · doi:10.32388/de0eae.2
Vérièpe-Salerno, J., Cancela, J. A., Vischer, S., Turzi, A., Cuendet, M., Giannopoulou, C., & Berndt, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.06.680686
Park, S.-R., Kim, S.-K., Kim, S.-R., Yu, W.-J., Lee, S.-J., & Lee, H.-Y. (2022) · Figshare · doi:10.6084/m9.figshare.20444283
Self-citationVérièpe-Salerno, J., Cancela, J. A., Vischer, S., Turzi, A., Cuendet, M., Giannopoulou, C., & Berndt, S. (2026) · Scientific Reports · doi:10.1038/s41598-026-38188-1
Advances in Oral Cavity Stem Cell Research Revealed through Multi-omics Analysis
Tsuchida, S., Umemura, H., Nakajima, M., Iizuka, K., Shimazaki, I., Shikata, E., & Nakayama, T. (2026) · Stem Cell Reviews and Reports · doi:10.1007/s12015-026-11119-3
Junttila, A., Heikkinen, J., Kylmäoja, E., Hawash, A., Åström, P., Lehenkari, P. P., & Palosaari, S. (2026) · Archives of Toxicology · doi:10.1007/s00204-026-04440-w
Louka, P., Pitsillides, A. A., Koumas, M., Papacharalambous, C., Sophocleous, A., & Zanos, P. (2026) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyag044
Oral nicotine pouch extracts disrupt osteogenic differentiation in human embryonic stem cells
Bertotto, L. B., Iwobi, N., Meletz, R. M., Zepeda, M., Khanal, K., Vera-Colón, M. K. M., & Sparks, N. R. L. (2026) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2026.118096
- Authors
- Kim, B.-S., Kim, S.-J., Kim, H.-J., Lee, S.-J., Park, Y.-J., Lee, J., & You, H.-K.
- Affiliations
- Wonkwang University (KR)
- Daegu Haany University (KR)
- Ewha Womans University (KR)
- Seoul National University (KR)
- Corresponding author
- Lee, Jun
- You, Hyung-Keun
- Venue
- Life Sciences
- Publisher
- Elsevier BV
- Published
- 2012-01
- Volume
- 90
- Issue
- 3-4
- Pages
- 109-115
- ISSN
- 0024-3205 (ISSN-L)
- OpenAlex
- W2029499588
- Cited by
- 98
- References
- 29
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 10 · 2023: 6 · 2022: 11 · 2021: 5 · 2020: 10 · 2019: 9 · 2018: 7 · 2017: 6 · 2016: 4 · 2015: 6 · 2014: 2 · 2013: 6 · 2012: 6
- FWCI
- 2.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Life Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fonds National de la Recherche Luxembourg
- National Research Foundation of Korea
- Topics
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
- Keywords
- nicotine, mesenchymal stem cells, osteogenic differentiation, cell proliferation, osteoporosis, alkaline phosphatase, Runx2, osteocalcin, bone sialoprotein, type I collagen, apoptosis, dose-dependent effects, periodontal disease
- MeSH terms
- Collagen Type I, alpha 1 Chain, Alveolar Process, Bone Marrow Cells, Cell Differentiation, Cells, Cultured, Dose-Response Relationship, Drug, Humans, Nicotine, Osteoblasts, Cell Proliferation, Mesenchymal Stem Cells
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