Skip to main content
Log in

Effect of Boron on Osteogenic Differentiation of Human Bone Marrow Stromal Cells

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Bone marrow stromal cells (BMSCs) have been well established as an ideal source of cell-based therapy for bone tissue engineering applications. Boron (B) is a notable trace element in humans; so far, the effects of boron on the osteogenic differentiation of BMSCs have not been reported. The aim of this study was to evaluate the effects of boron (0, 1, 10,100, and 1,000 ng/ml) on osteogenic differentiation of human BMSCs. In this study, BMSCs proliferation was analyzed by cell counting kit-8 (CCK8) assay, and cell osteogenic differentiation was evaluated by alkaline phosphatase (ALP) activity assay, Von Kossa staining, and real-time PCR. The results indicated that the proliferation of BMSCs was no different from the control group when added with B at the concentration of 1, 10, and 100 ng/ml respectively (P > 0.05); in contrast, 1,000 ng/ml B inhibited the proliferation of BMSCs at days 4, 7, and 14 (P < 0.05). By ALP staining, we discovered that BMSCs treated with 10 and 100 ng/ml B presented a higher ALP activity compared with control (P < 0.05). By real-time PCR, we detected the messenger RNA expression of ALP, osteocalcin, collagen type I, and bone morphogenetic proteins 7 were also increased in 10 and 100 ng/ml B treatment groups (P < 0.05). The calcium depositions were increased in 1 and 10 ng/ml B treatment groups (P < 0.05). Taken all together, it was the first time to report that B could increase osteogenic effect by stimulating osteogenic differentiation-related marker gene synthesis during the proliferation and differentiation phase in human BMSCs and could be a promising approach for enhancing osteogenic capacity of cell-based construction in bone tissue engineering.

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

Access this article

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. Nielsen FH (2000) The emergence of boron as nutritionally important throughout the life cycle. Nutrition 16(7–8):512–514

    Article  PubMed  CAS  Google Scholar 

  2. Nielsen FH (1998) The justification for providing dietary guidance for the nutritional intake of boron. Biol Trace Elem Res 66(1–3):319–330

    Article  PubMed  CAS  Google Scholar 

  3. Hunt CD, Nielsen FH (1981) Interaction between boron and cholecalciferol in the chick. In: McCHowell J, Gawthorne JM, White CL (eds) Trace element metabolism in man and animals (TEMA-4). Australia:Australian Academy of Science, Canberra, pp 597–600

    Chapter  Google Scholar 

  4. Nielsen FH (2004) Dietary fat composition modifies the effect of B on bone characteristics and plasma lipids in rats. Biofactors 20:161–171

    Article  PubMed  CAS  Google Scholar 

  5. Gallardo-Williams MT, Maronpot RR, Turner CH, Johnson CS, Harris MW, Jayo MJ (2003) Effects of boric acid supplementation on bone histomorphometry, metabolism, and biomechanical properties in aged female F-344 rats. Biol Trace Elem Res 93:155–169

    Article  PubMed  CAS  Google Scholar 

  6. Devirian TA, Volpe SL (2003) The physiological effects of dietary boron. Crit Rev Food Sci Nutr 43:219–231

    Article  PubMed  CAS  Google Scholar 

  7. Gorustovich AA, Steimetz T, Nielsen FH, Guglielmotti MB (2008) A histomorphometric study of alveolar bone modeling and remodeling in mice fed a boron-deficient diet. Arch Oral Biol 53:677–682

    Article  PubMed  CAS  Google Scholar 

  8. Chapin RE, Ku WW, Kenney MA, McCoy H (1998) The effects of dietary boric acid on bone strength in rats. Biol Trace Elem Res 66:395–399

    Article  PubMed  CAS  Google Scholar 

  9. Gorustovich AA, López JM, Guglielmotti MB, Cabrini RL (2006) Biological performance of boron-modified bioactive glass particles implanted in rat tibia bone marrow. Biomed Mater 1(3):100–105

    Article  PubMed  CAS  Google Scholar 

  10. Xie Z, Liu X, Jia W, Zhang C, Huang W, Wang J (2009) Treatment of osteomyelitis and repair of bone defect by degradable bioactive borate glass releasing vancomycin. J Control Release 139(2):118–126

    Article  PubMed  CAS  Google Scholar 

  11. Food and Nutrition Board, Standing Committee on the Scientific Evaluation of Dietary Reference Intake, Institute of Medicine (2002) Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium and zinc. National Academy Press, Washington

  12. Meacham SL, Taper LJ, Volpe SL (1994) Effects of boron supplementation on bone mineral density and dietary, blood, and urinary calcium, phosphorus, magnesium, and boron in female athletes. Environ Health Perspect 102(suppl7):79–82

    PubMed  CAS  Google Scholar 

  13. Sheng MH-C, Taper LJ, Veit H, Qian H, Ritchey SJ, Lau K-HW (2001) Dietary boron supplementation enhanced theaction of estrogen, but not that of parathyroid hormone, to improve trabecular bone quality in ovariectomized rats. Biol Trace Elem Res 82:109–123

    Article  PubMed  CAS  Google Scholar 

  14. Hakki SS, Bozkurt BS, Hakki EE (2010) Boron regulates mineralized tissue-associated proteins in osteoblasts (MC3T3-E1). J Trace Elem Med Biol 24(4):243–250

    Article  PubMed  CAS  Google Scholar 

  15. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9:641–650

    Article  PubMed  CAS  Google Scholar 

  16. Park M, Li Q, Shcheynikov N, Zeng WZ, Muallem S (2004) NABC1 is a ubiquitous electrogenic Na+-coupled borate transporter essential for cellular boron homeostasis and cell growth and proliferation. Mol Cell 16:331–341

    Article  PubMed  CAS  Google Scholar 

  17. Liu Y, Tan J, Li L, Li S, Zou S, Zhang Y et al (2010) Study on the molecular mechanisms of dlk1 stimulated lung cancer cell proliferation. Zhongguo Fei Ai Za Zhi 13(10):923–927

    PubMed  CAS  Google Scholar 

  18. Kasten P, Luginbühl R, van Griensven M, Barkhausen T, Krettek C, Bohner M et al (2003) Comparison of human bone marrow stromal cells seeded on calcium-deficient hydroxyapatite, beta-tricalcium phosphate and demineralized bone matrix. Biomaterials 24:2593–2603

    Article  PubMed  CAS  Google Scholar 

  19. Sun H, Wu C, Dai K, Chang J, Tang T (2006) Proliferation and osteoblastic differentiation of human bone marrow-derived stromal cells on akermanite-bioactive ceramics. Biomaterials 27:5651–5657

    Article  PubMed  CAS  Google Scholar 

  20. Hunt CD (1998) One possible role of dietary boron in higher animals and humans. Biol Tr Elem Res 66:205–225

    Article  CAS  Google Scholar 

  21. Nielsen FH (2000) Evolutionary events culminating in specific minerals becoming essential for life. Eur J Nutr 39(2):62–66

    Article  PubMed  CAS  Google Scholar 

  22. Sutherland B, Strong P, King JC (1998) Determining human dietary requirements for boron. Biol Tr Elem Res 66:193–204

    Article  CAS  Google Scholar 

  23. Brown RF, Rahaman MN, Dwilewicz AB, Huang W, Day DE, Li Y (2009) Effect of borate glass composition on its conversion to hydroxyapatite and on the proliferation of MC3T3-E1 cells. J Biomed Mater Res A 88(2):392–400

    PubMed  Google Scholar 

  24. Zou L, Zou X, Chen L, Li H, Mygind T, Kassem M et al (2008) Multilineage differentiation of porcine bone marrow stromal cells associated with specific gene expression pattern. J Orthop Res 26:56–64

    Article  PubMed  CAS  Google Scholar 

  25. Serigano K, Sakai D, Hiyama A, Tamura F, Tanaka M, Mochida J (2010) Effect of cell number on mesenchymal stem cell transplantation in a canine disc degeneration model. J Orthop Res 28:1267–1275

    Article  PubMed  Google Scholar 

  26. Stucki U, Schmid J, Hammerle CF, Lang NP (2001) Temporal and local appearance of alkaline phosphatase activity in early stages of guided bone regeneration. A descriptive histochemical study in humans. Clin Oral Implants Res 12:121–127

    Article  PubMed  CAS  Google Scholar 

  27. Luu HH, Song WX, Luo X, Manning D, Luo J, Deng ZL et al (2007) Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells. J Orthop Res 25:665–677

    Article  PubMed  CAS  Google Scholar 

  28. Hauschka PV, Lian JB, Cole DE, Gundberg CM (1989) Osteocalcin and matrix Gla protein:vitamin K-dependent proteins in bone. Physiol Rev 69:990–1047

    PubMed  CAS  Google Scholar 

  29. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS et al (1990) Progressive development of the rat osteoblast phenotype in vitro:reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 143:420–430

    Article  PubMed  CAS  Google Scholar 

  30. Nzietchueng RM, Dousset B, Franck P, Benderdour M, Nabet P, Hess K (2002) Mechanisms implicated in the effects of boron on wound healing. J Trace Elem Med Biol 16(4):239–244

    Article  PubMed  CAS  Google Scholar 

  31. Benderdour M, Van Bui T, Hess K, Dicko A, Belleville F, Dousset B (2000) Effects of boron derivatives on extracellular matrix formation. J Trace Elem Med Biol 14(3):168–173

    Article  PubMed  CAS  Google Scholar 

  32. Armstrong TA, Spears JW (2001) Effect of dietary boron on growth performance, calcium and phosphorus metabolism, and bone mechanical properties in growing barrows. J Anim Sci 79(12):3120–3127

    PubMed  CAS  Google Scholar 

  33. Komori T (2006) Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 99:1233–1239

    Article  PubMed  CAS  Google Scholar 

  34. Wang A, Ding X, Sheng S, Yao Z (2010) Bone morphogenetic protein receptor in the osteogenic differentiation of rat bone marrow stromal cells. Yonsei Med J 51:740–745

    Article  PubMed  CAS  Google Scholar 

  35. Chen D, Zhao M, Mundy GR (2004) Bone morphogenetic proteins. Growth Factors 22:233–241

    Article  PubMed  CAS  Google Scholar 

  36. Chimal-Monroy J, Rodriguez-Leon J, Montero JA, Ganan Y, Macias D, Merino R et al (2003) Analysis of the molecular cascade responsible for mesodermal limb chondrogenesis: Sox genes and BMP signaling. Dev Biol 257:292–301

    Article  PubMed  CAS  Google Scholar 

  37. Wozney JM (2002) Overview of bone morphogenetic proteins. Spine 27:2–8

    Article  Google Scholar 

  38. Biase PD, Capanna R (2005) Clinical applications of BMPs. Injury 36:43–46

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank all the staff in the Laboratory of Orthopaedic Research Institute and Scientific Research Center of Second Affiliated Hospital of Wenzhou Medical College. This work was supported by grants from the National Natural Science Foundation of China (30800220/C100201).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Lei Peng or Chuan zhu Lu.

Additional information

X. Ying and S. Cheng contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ying, X., Cheng, S., Wang, W. et al. Effect of Boron on Osteogenic Differentiation of Human Bone Marrow Stromal Cells. Biol Trace Elem Res 144, 306–315 (2011). https://doi.org/10.1007/s12011-011-9094-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-011-9094-x

Keywords

Navigation