Skip to main content
SpringerLink
Log in

Green tea protects human osteoblasts from cigarette smoke-induced injury: possible clinical implication

  • Original Article
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Purpose

Recent reports discuss the altered bone homeostasis in cigarette smokers, being a risk factor for osteoporosis and negatively influencing fracture healing. Cigarette smoke is known to induce oxidative stress in the body via an increased production of reactive oxygen species (ROS). These increases in ROS are thought to damage the bone-forming osteoblasts. Naturally occurring polyphenols contained in green tea extract (GTE), e.g., catechins, are known to have anti-oxidative properties. Therefore, the aim of this study was to investigate whether GTE and especially catechins protect primary human osteoblasts from cigarette smoke-induced damage and to identify the underlying mechanisms.

Methods

Primary human osteoblasts were isolated from patients’ femur heads. Cigarette smoke medium (CSM) was obtained using a gas-washing bottle and standardized by its optical density (OD320) at λ = 320 nm. ROS formation was measured using 2′7′dichlorofluorescein diacetate, and osteoblasts’ viability was detected by resazurin conversion.

Results

Co-, pre-, and post-incubation with GTE and catechins significantly reduced ROS formation and thus improved the viability of CSM-treated osteoblasts. Besides GTE’s direct radical scavenging properties, pre-incubation with both GTE and catechins protected osteoblasts from CSM-induced damage. Inhibition of the anti-oxidative enzyme HO-1 significantly reduced the protective effect of GTE and catechins emphasizing the key role of this enzyme in GTE anti-oxidative effect.

Conclusions

Our data suggest possible beneficial effects on bone homeostasis, fracture healing, and bone mineral density following a GTE-rich diet or supplementation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3(Suppl 3):S131–S139

    Article  PubMed  CAS  Google Scholar 

  2. Nijweide PJ et al (1986) Cells of bone: proliferation, differentiation, and hormonal regulation. Physiol Rev 66:855–886

    PubMed  CAS  Google Scholar 

  3. Akhter MP et al (2005) Bone biomechanical property deterioration due to tobacco smoke exposure. Calcif Tissue Int 77:319–326

    Article  PubMed  CAS  Google Scholar 

  4. Cesar-Neto JB et al (2005) The influence of cigarette smoke inhalation on bone density. A radiographic study in rats. Braz Oral Res 19:47–51

    Article  PubMed  Google Scholar 

  5. Cesar-Neto JB et al (2006) The influence of cigarette smoke inhalation and its cessation on the tooth-supporting alveolar bone: a histometric study in rats. J Periodontal Res 41:118–123

    Article  PubMed  Google Scholar 

  6. Cesar-Neto JB et al (2003) A comparative study on the effect of nicotine administration and cigarette smoke inhalation on bone healing around titanium implants. J Periodontol 74:1454–1459

    Article  PubMed  CAS  Google Scholar 

  7. Rapuri PB et al (2000) Smoking and bone metabolism in elderly women. Bone 27:429–436

    Article  PubMed  CAS  Google Scholar 

  8. Schmitz MA et al. (1999) Effect of smoking on tibial shaft fracture healing. Clin Orthop Relat Res 365:184–200

    Google Scholar 

  9. Ward KD, Klesges RC (2001) A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int 68:259–270

    Article  PubMed  CAS  Google Scholar 

  10. Rothem DE et al (2009) Nicotine modulates bone metabolism-associated gene expression in osteoblast cells. J Bone Miner Metab 27:555–561

    Article  PubMed  CAS  Google Scholar 

  11. Ajiro Y et al (2010) Impact of passive smoking on the bones of rats. Orthopedics 33:90–95

    Article  PubMed  Google Scholar 

  12. Ueng SW et al (1999) Hyperbaric oxygen therapy mitigates the adverse effect of cigarette smoking on the bone healing of tibial lengthening: an experimental study on rabbits. J Trauma 47:752–759

    Article  PubMed  CAS  Google Scholar 

  13. Ueng SW et al (1999) Bone healing of tibial lengthening is delayed by cigarette smoking: study of bone mineral density and torsional strength on rabbits. J Trauma 46:110–115

    Article  PubMed  CAS  Google Scholar 

  14. Nakamura Y et al (1995) Cigarette smoke inhibits lung fibroblast proliferation and chemotaxis. Am J Respir Crit Care Med 151:1497–1503

    PubMed  CAS  Google Scholar 

  15. Wang H et al (2001) Cigarette smoke inhibits human bronchial epithelial cell repair processes. Am J Respir Cell Mol Biol 25:772–779

    PubMed  CAS  Google Scholar 

  16. Willey JC et al (1987) Biochemical and morphological effects of cigarette smoke condensate and its fractions on normal human bronchial epithelial cells in vitro. Cancer Res 47:2045–2049

    PubMed  CAS  Google Scholar 

  17. Cesar-Neto JB et al (2007) Smoking modulates interleukin-6:interleukin-10 and RANKL:osteoprotegerin ratios in the periodontal tissues. J Periodontal Res 42:184–191

    Article  PubMed  CAS  Google Scholar 

  18. Giorgetti AP et al. (2010) Cigarette smoke inhalation modulates gene expression in sites of bone healing: a study in rats. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 110:447–452

    Google Scholar 

  19. Kim H et al (2004) Reversible cigarette smoke extract-induced DNA damage in human lung fibroblasts. Am J Respir Cell Mol Biol 31:483–490

    Article  PubMed  CAS  Google Scholar 

  20. Mortaz E et al (2009) Effect of cigarette smoke extract on dendritic cells and their impact on T-cell proliferation. PLoS One 4:e4946

    Article  PubMed  Google Scholar 

  21. Bai XC et al (2004) Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF–kappaB. Biochem Biophys Res Commun 314:197–207

    Article  PubMed  CAS  Google Scholar 

  22. Bai XC et al (2005) Reactive oxygen species stimulates receptor activator of NF–kappaB ligand expression in osteoblast. J Biol Chem 280:17497–17506

    Article  PubMed  CAS  Google Scholar 

  23. Gonzalez-Gallego J et al. (2010) Fruit polyphenols, immunity and inflammation. Br J Nutr 104(Suppl 3):S15–27

    Google Scholar 

  24. Gonzalez-Gallego J et al (2007) Anti-inflammatory properties of dietary flavonoids. Nutr Hosp 22:287–293

    PubMed  CAS  Google Scholar 

  25. Russo A et al (2000) Bioflavonoids as antiradicals, antioxidants and DNA cleavage protectors. Cell Biol Toxicol 16:91–98

    Article  PubMed  CAS  Google Scholar 

  26. Gawlik M, Czajka A (2007) The effect of green, black and white tea on the level of alpha and gamma tocopherols in free radical-induced oxidative damage of human red blood cells. Acta Pol Pharm 64:159–164

    PubMed  CAS  Google Scholar 

  27. Relja B et al. (2011) Effects of green tea catechins on the pro-inflammatory response after haemorrhage/resuscitation in rats. Br J Nutr 4:1–7

    Google Scholar 

  28. Shen CL et al. (2010) Protective actions of green tea polyphenols and alfacalcidol on bone microstructure in female rats with chronic inflammation. J Nutr Biochem 22:673-680

    Google Scholar 

  29. Shen CL et al (2008) Protective effect of green tea polyphenols on bone loss in middle-aged female rats. Osteoporos Int 19:979–990

    Article  PubMed  CAS  Google Scholar 

  30. Wu CH et al (2002) Epidemiological evidence of increased bone mineral density in habitual tea drinkers. Arch Intern Med 162:1001–1006

    Article  PubMed  Google Scholar 

  31. Bao W et al (2010) Curcumin alleviates ethanol-induced hepatocytes oxidative damage involving heme oxygenase-1 induction. J Ethnopharmacol 128:549–553

    Article  PubMed  CAS  Google Scholar 

  32. Yao P et al (2007) Heme oxygenase-1 upregulated by Ginkgo biloba extract: potential protection against ethanol-induced oxidative liver damage. Food Chem Toxicol 45:1333–1342

    Article  PubMed  CAS  Google Scholar 

  33. Yao P et al (2007) Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J Hepatol 47:253–261

    Article  PubMed  CAS  Google Scholar 

  34. Farombi EO, Surh YJ (2006) Heme oxygenase-1 as a potential therapeutic target for hepatoprotection. J Biochem Mol Biol 39:479–491

    Article  PubMed  CAS  Google Scholar 

  35. Barbagallo I et al (2011) Overexpression of heme oxygenase-1 increases human osteoblast stem cell differentiation. J Bone Miner Metab 28:276–288

    Article  Google Scholar 

  36. Komatsu DE, Hadjiargyrou M (2004) Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair. Bone 34:680–688

    Article  PubMed  CAS  Google Scholar 

  37. Ehnert S et al (2010) TGF-beta1 as possible link between loss of bone mineral density and chronic inflammation. PLoS One 5:e14073

    Article  PubMed  Google Scholar 

  38. El-Amin SF et al (2006) Human osteoblast cells: isolation, characterization, and growth on polymers for musculoskeletal tissue engineering. J Biomed Mater Res A 76:439–449

    PubMed  Google Scholar 

  39. Roemer E et al (2004) Chemical composition, cytotoxicity and mutagenicity of smoke from US commercial and reference cigarettes smoked under two sets of machine smoking conditions. Toxicology 195:31–52

    Article  PubMed  CAS  Google Scholar 

  40. Lin S et al (2009) Comparison of toxicity of smoke from traditional and harm-reduction cigarettes using mouse embryonic stem cells as a novel model for preimplantation development. Hum Reprod 24:386–397

    Article  PubMed  CAS  Google Scholar 

  41. Luppi F et al (2005) Effects of cigarette smoke condensate on proliferation and wound closure of bronchial epithelial cells in vitro: role of glutathione. Respir Res 6:140

    Article  PubMed  Google Scholar 

  42. Wirtz HR, Schmidt M (1996) Acute influence of cigarette smoke on secretion of pulmonary surfactant in rat alveolar type II cells in culture. Eur Respir J 9:24–32

    Article  PubMed  CAS  Google Scholar 

  43. Sarkar M et al (2006) Flow-cytometric analysis of reactive oxygen species in peripheral blood mononuclear cells of patients with thyroid dysfunction. Cytometry B Clin Cytom 70:20–23

    PubMed  Google Scholar 

  44. Iwaniec UT et al (2001) Effects of nicotine on bone mass, turnover, and strength in adult female rats. Calcif Tissue Int 68:358–364

    Article  PubMed  CAS  Google Scholar 

  45. Lee LL et al (2002) Polycyclic aromatic hydrocarbons present in cigarette smoke cause bone loss in an ovariectomized rat model. Bone 30:917–923

    Article  PubMed  CAS  Google Scholar 

  46. Aoshiba K, Nagai A (2003) Oxidative stress, cell death, and other damage to alveolar epithelial cells induced by cigarette smoke. Tob Induc Dis 1:219–226

    Article  PubMed  CAS  Google Scholar 

  47. Devine A et al (2007) Tea drinking is associated with benefits on bone density in older women. Am J Clin Nutr 86:1243–1247

    PubMed  CAS  Google Scholar 

  48. Hamdi Kara I et al (2007) Habitual tea drinking and bone mineral density in postmenopausal Turkish women: investigation of prevalence of postmenopausal osteoporosis in Turkey (IPPOT Study). Int J Vitam Nutr Res 77:389–397

    Article  PubMed  Google Scholar 

  49. Hegarty VM et al (2000) Tea drinking and bone mineral density in older women. Am J Clin Nutr 71:1003–1007

    PubMed  CAS  Google Scholar 

  50. Shen CL et al (2009) Green tea polyphenols and Tai Chi for bone health: designing a placebo-controlled randomized trial. BMC Musculoskelet Disord 10:110

    Article  PubMed  Google Scholar 

  51. Shen CL et al (2009) Green tea and bone metabolism. Nutr Res 29:437–456

    Article  PubMed  CAS  Google Scholar 

  52. Chae HJ et al (2006) Carbon monoxide and nitric oxide protect against tumor necrosis factor-alpha-induced apoptosis in osteoblasts: HO-1 is necessary to mediate the protection. Clin Chim Acta 365:270–278

    Article  PubMed  CAS  Google Scholar 

  53. Lin TH et al (2011) Upregulation of heme oxygenase-1 inhibits the maturation and mineralization of osteoblasts. J Cell Physiol 222:757–768

    Google Scholar 

  54. Basu S et al (2001) Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun 288:275–279

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of interest

None.

Author information

Authors and Affiliations

  1. Department of Traumatology, MRI, Technische Universität München, Munich, Germany

    Nina Holzer, Karl F. Braun, Arne Buchholz, Lilianna Schyschka, Markus Neumaier & Andreas K. Nussler

  2. BG Trauma Center, Eberhard Karls Universität Tübingen, Schnarrenbergstr. 95, 72076, Tübingen, Germany

    Sabrina Ehnert, Ulrich Stöckle, Thomas Freude & Andreas K. Nussler

  3. Department of Plastic Surgery and Hand Surgery, Technische Universität München, Munich, Germany

    José T. Egaña & Thilo L. Schenck

  4. FONDAP Center for Genome Regulation, Facultad de Ciencias, Universidad de Chile, Santiago, Chile

    José T. Egaña

  5. Fresenius Kabi GmbH, Oberursel, Germany

    Steffen Benzing

Authors
  1. Nina Holzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karl F. Braun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sabrina Ehnert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José T. Egaña
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thilo L. Schenck
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arne Buchholz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lilianna Schyschka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Markus Neumaier
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Steffen Benzing
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ulrich Stöckle
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Thomas Freude
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Andreas K. Nussler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas K. Nussler.

Additional information

Nina Holzer, Karl F. Braun, Sabrina Ehnert, Thomas Freude, and Andreas K. Nussler contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holzer, N., Braun, K.F., Ehnert, S. et al. Green tea protects human osteoblasts from cigarette smoke-induced injury: possible clinical implication. Langenbecks Arch Surg 397, 467–474 (2012). https://doi.org/10.1007/s00423-011-0882-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-011-0882-8

Keywords

Search

Navigation