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Biological Trace Element Research

, Volume 188, Issue 1, pp 221–229 | Cite as

Effects of Nutritional Deficiency of Boron on the Bones of the Appendicular Skeleton of Mice

  • Alejandro A. GorustovichEmail author
  • Forrest H. Nielsen
Article
  • 34 Downloads

Abstract

Scientific evidence has shown the nutritional importance of boron (B) in the remodeling and repair of cancellous bone tissue. However, the effects of the nutritional deficiency of B on the cortical bone tissue of the appendicular skeleton have not yet been described. Thus, a study was performed to histomorphometrically evaluate the density of osteocyte lacunae of cortical bone of mouse femora under conditions of nutritional deficiency of B and to analyze the effects of the deficiency on the biomechanical properties of mouse tibiae. Weaning, 21-day-old male Swiss mice were assigned to the following two groups: controls (B+; n = 10) and experimental (B−; n = 10). Control mice were fed a basal diet containing 3 mg B/kg, whereas experimental mice were fed a B-deficient diet containing 0.07 mg B/kg for 9 weeks. The histological and histomorphometric evaluations of the mice fed a B-deficient diet showed a decrease in the density of osteocyte lacunae in the femoral cortical bone tissue and the evaluation of biomechanical properties showed lower bone rigidity in the tibia.

Keywords

Boron Cortical bone Osteocyte lacunae Histomorphometry Biomechanical properties 

Notes

Acknowledgements

The authors wish to acknowledge the technical assistance of Jim Lindlauf (USDA ARS, Grand Forks Human Nutrition Research Center) for the preparation of the animal diets and Lic. Pablo Do Campo (IByME-CONICET) for the confocal laser scanning microscopy.

Funding Information

This study was supported by the United States Department of Agriculture, Agriculture Research Service USDA, ARS Extramural Agreement 58-5450-4N-F038.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. 1.
    Boskey AL, Gehron-Robey P (2013) The composition of bone. In: Rosen CJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism, 8th edn. American Society for Bone and Mineral Research, John Wiley & Sons, New York, pp 49–58Google Scholar
  2. 2.
    Bonewald LF (2011) The amazing osteocyte. J Bone Miner Res 26:229–238Google Scholar
  3. 3.
    Noble BS (2008) The osteocyte lineage. Arch Biochem Biophys 473:106–111Google Scholar
  4. 4.
    Franz-Odendaal TA, Hall BK, Witten PE (2006) Burried alive: how osteoblasts become osteocytes. Dev Dyn 235:176–190Google Scholar
  5. 5.
    Marie PJ, Cohen-Solal M (2018) The expanding life and functions of osteogenic cells: from simple bone-making cells to multifunctional cells and beyond. J Bone Miner Res 33:199–210Google Scholar
  6. 6.
    Bonewald LF, Johnson ML (2008) Osteocytes, mechanosensing and Wnt signaling. Bone 42:606–615Google Scholar
  7. 7.
    Aarden EM, Burger EH, Nijweide PJ (1994) Function of osteocytes in bone. J Cell Biochem 55:287–299Google Scholar
  8. 8.
    Knothe Tate ML, Adamson JR, Tami AE, Bauer TW (2004) The osteocyte. Int J Biomed Cell Biol 36:1–8Google Scholar
  9. 9.
    Fukumoto S, Martin TJ (2009) Bone as an endocrine organ. Trends Endocrinol Metab 20:230–236Google Scholar
  10. 10.
    Dallas SL, Prideaux M, Bonewald LF (2013) The osteocyte: an endocrine cell ... and more. Endocr Rev 34:658–690Google Scholar
  11. 11.
    Manolagas SC, Parfitt AM (2013) For whom the bell tolls: distress signals from long-lived osteocytes and the pathogenesis of metabolic bone diseases. Bone 54:272–278Google Scholar
  12. 12.
    Sapir-Koren R, Livshits G (2014) Bone mineralization is regulated by signaling cross talk between molecular factors of local and systemic origin: the role of fibroblast growth factor 23. Biofactors 40:555–568Google Scholar
  13. 13.
    Bellido T (2014) Osteocyte-driven bone remodeling. Calcif Tissue Int 94:25–34Google Scholar
  14. 14.
    Plotkin LI, Bellido T (2016) Osteocytic signalling pathways as therapeutic targets for bone fragility. Nat Rev Endocrinol 12:593–605Google Scholar
  15. 15.
    Bonewald LF (2017) The role of the osteocyte in bone and nonbone disease. Endocrinol Metab Clin N Am 46:1–18Google Scholar
  16. 16.
    Hemmatian H, Bakker AD, Klein-Nulend J, van Lenthe GH (2017) Aging, osteocytes, and mechanotransduction. Curr Osteoporos Rep 15:401–411Google Scholar
  17. 17.
    Uda Y, Azab E, Sun N, Shi C, Pajevic PD (2017) Osteocyte mechanobiology. Curr Osteoporos Rep 15:318–325Google Scholar
  18. 18.
    Hall BK (2005) Bones and cartilage: developmental and evolutionary skeletal biology. Elsevier Academic Press, San DiegoGoogle Scholar
  19. 19.
    Teti A, Zallone A (2009) Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44:11–16Google Scholar
  20. 20.
    Nielsen FH (2000) Importance of making dietary recommendations of elements designates as nutritionally beneficial, pharmacologically beneficial, or conditionally essential. J Trace Elem Exp Med 13:113–129Google Scholar
  21. 21.
    Nieves JW (2005) Osteoporosis: the role of micronutrients. Am J Clin Nutr 81:1232S–1239SGoogle Scholar
  22. 22.
    Palacios C (2006) The role of nutrients in bone health, from A to Z. Crit Rev Food Sci Nutr 46:621–628Google Scholar
  23. 23.
    Prentice A, Schoenmakers I, Laskey MA, de Bono S, Ginty F, Goldberg GR (2006) Nutrition and bone growth and development. Proc Nutr Soc 65:348–360Google Scholar
  24. 24.
    Heaney RP (2007) Bone health. Am J Clin Nutr 85:300S–303SGoogle Scholar
  25. 25.
    Bonjour JP, Guéguen L, Palacios C, Shearer MJ, Weaven CM (2009) Minerals and vitamins in bone health: the potential value of dietary enhancement. Br J Nutr 101:1581–1596Google Scholar
  26. 26.
    Zofkova I, Davis M, Blahos J (2017) Trace elements have beneficial, as well as detrimental effects on bone homeostasis. Physiol Res 66:391–402Google Scholar
  27. 27.
    Nielsen FH (2000) The emergence of boron as nutritionally important throughout the life cycle. Nutrition 16:512–514Google Scholar
  28. 28.
    Nielsen FH (2002) The nutritional importance and pharmacological potential of boron for higher animals and human. In: Goldbach HE, Brown PH, Rerkasem B, Thellier M, Wimmer MA, Bell RW (eds) Boron in plant and animal nutrition. Springer, Boston, pp 37–49Google Scholar
  29. 29.
    Devirian TA, Volpe SL (2003) The physiological effects of dietary boron. Crit Rev Food Sci Nutr 43:219–231Google Scholar
  30. 30.
    Park M, Li Q, Shcheynikov N, Muallem S, Zeng W (2005) Borate transport and cell growth and proliferation. Cell Cycle 4:24–26Google Scholar
  31. 31.
    Nielsen FH (2008) Is boron nutritionally relevant? Nutr Rev 66:183–191Google Scholar
  32. 32.
    Hunt CD (2008) Dietary boron: possible roles in human and animal physiology. Biomed Res Trace Elem 19:243–253Google Scholar
  33. 33.
    Hunt CD (2012) Dietary boron: progress in establishing essential roles in human physiology. J Trace Elem Med Biol 26:157–160Google Scholar
  34. 34.
    Nielsen FH (2014) Update on human health effects of boron. J Trace Elem Med Biol 28:383–387Google Scholar
  35. 35.
    Khaliq H, Juming Z, Ke-Mei P (2018) The physiological role of boron on health. Biol Trace Elem Res.  https://doi.org/10.1007/s12011-018-1284-3
  36. 36.
    Uluisik I, Karakaya HC, Koc A (2018) The importance of boron in biological systems. J Trace Elem Med Biol 45:156–162Google Scholar
  37. 37.
    Sheng MH, Taper LJ, Veit H, Thomas EA, Ritchey SJ, Lau KH (2001) Dietary boron supplementation enhances the effects of estrogen on bone mineral balance in ovariectomized rats. Biol Trace Elem Res 81:29–45Google Scholar
  38. 38.
    Gallardo-Williams MT, Maronpot RR, Turner CH, Jonson CS, Harris MW, Jayo ML, Chapin RE (2003) Effects of boric acid supplementation on bone histomorphometry, metabolism, and biomechanical properties in aged female F-344 rats. Biol Trace Elem Res 3:155–169Google Scholar
  39. 39.
    Gorustovich A, Steimetz T, Nielsen FH, Guglielmotti MB (2008) Histomorphometric study of alveolar bone healing in rats fed a boron-deficient diet. Anat Rec 291:441–447Google Scholar
  40. 40.
    Nielsen FH, Stoeker BJ (2009) Boron and fish oil have different beneficial effects on strength and trabecular microarchitecture of bone. J Trace Elem Med Biol 23:195–203Google Scholar
  41. 41.
    Gorustovich A, 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 53:677–682Google Scholar
  42. 42.
    Wink CS, Rossowka MJ, Nakamoto T (1996) Effects of caffeine on bone cells and bone development in fast-growing rats. Anat Rec 246:30–38Google Scholar
  43. 43.
    Bentolia V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB (1998) Intarcortical remodeling in adult rat long bones after fatigue loading. Bone 23:275–281Google Scholar
  44. 44.
    Tomkinson A, Gevers EF, Wit JM, Reeve J, Noble BS (1998) The role of estrogen in the control of rat osteocyte apoptosis. J Bone Miner Res 13:1243–1250Google Scholar
  45. 45.
    Ohta M, Cheuk G, Thomas KV, Kamagata-Kiyoura Y, Wink CS, Yazdani M, Falster AU, Simmons WB, Nakamoto T (1999) Effects of caffeine on the bones of aged, ovariectomized rats. Ann Nutr Metab 43:52–59Google Scholar
  46. 46.
    Vashishth D, Verborgt O, Divine G, Schaffler MB, Fyhrie DP (2000) Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. Bone 26:375–380Google Scholar
  47. 47.
    Vashishth D, Gibson G, Kimura J, Schaffler MB, Pyhrie DP (2002) Determination of bone volume by osteocyte population. Anat Rec 267:292–295Google Scholar
  48. 48.
    Qiu S, Rao DS, Palnitkar S, Parfitt AM (2002) Age and distance from the surface but not menopause reduce osteocyte density in human cancellous bone. Bone 31:313–318Google Scholar
  49. 49.
    Qiu S, Rao DS, Palnitkar S, Parfitt AM (2002) Relationships between osteocyte density and bone formation rate in human cancellous bone. Bone 31:709–711Google Scholar
  50. 50.
    Qiu S, Fyhrie DP, Palnitkar S, Rao DS (2003) Histomorphometric assessment of Haversian canal and osteocyte lacunae in different-sized osteons in human rib. Anat Rec A Discov Mol Cell Evol Biol 272:520–525Google Scholar
  51. 51.
    Qiu S, Rao DS, Palnitkar S, Parfitt AM (2003) Reduced iliac cancellous osteocyte density in patients with osteoporotic vertebral fracture. J Bone Miner Res 18:1657–1663Google Scholar
  52. 52.
    Qiu S, Rao DS, Fyhrie DP, Palnitkar S, Parfitt AM (2005) The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37:10–15Google Scholar
  53. 53.
    Qiu S, Rao D, Fyhrie DP, Palnitkar S, Parfitt AM (2006) Differences in osteocyte and lacunar density between Black and White American women. Bone 38:130–135Google Scholar
  54. 54.
    Iwamoto J, Matsumoto H, Takeda T, Sato Y, Liu X, Yeh JK (2008) Effects of vitamin K2 and risedronate on bone formation and resorption, osteocyte lacunar system, and porosity in the cortical bone of glucocorticoid-treated rats. Calcif Tissue Int 83:121–128Google Scholar
  55. 55.
    Dai R, Ma Y, Sheng Z, Jin Y, Zhang Y, Fang L, Fan H, Liao E (2008) Effects of genistein on vertebral trabecular bone microstructure, bone mineral density, microcracks, osteocyte density, and bone strength in ovariectomized rats. J Bone Miner Metab 26:342–349Google Scholar
  56. 56.
    Rawlinson SCF, Boyde A, Davis GR, Howell PGT, Hughes FJ, Kingsmill VJ (2009) Ovariectomy vs. hypofunction: their effects on rat mandibular bone. J Dent Res 88:615–620Google Scholar
  57. 57.
    Skedros JG, Clark GC, Sorenson SM, Taylor KW, Qiu S (2011) Analysis of the effect of osteon diameter on the potential relationship of osteocyte lacuna density and osteon wall thickness. Anat Rec (Hoboken) 294:1472–1485Google Scholar
  58. 58.
    Sharma D, Ciani C, Marin PA, Levy JD, Doty SB, Fritton SP (2012) Alterations in the osteocyte lacunar-canalicular microenvironment due to estrogen deficiency. Bone 51:488–497Google Scholar
  59. 59.
    Stern AR, Yao X, Wang Y, Berhe A, Dallas M, Johnson ML, Yao W, Kimmel DB, Lane NE (2018) Effect of osteoporosis treatment agents on the cortical bone osteocyte microenvironment in adult estrogen-deficient, osteopenic rats. Bone Rep 26:115–124Google Scholar
  60. 60.
    Hemmatian H, Laurent MR, Bakker AD, Vanderschueren D, Klein-Nulend J, van Lenthe GH (2018) Age-related changes in female mouse cortical bone microporosity. Bone 113:1–8Google Scholar
  61. 61.
    Nielsen FH (2004) Dietary fat composition modifies the effect of boron on bone characteristics and plasma lipids in rats. Biofactors 20:161–171Google Scholar
  62. 62.
    Frost HM (1960) Presence of microscopic cracks in vivo in bone. Henry Ford Hosp Med Bull 8:25–35Google Scholar
  63. 63.
    Burr DF, Stafford T (1990) Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage. Clin Orthop Relat Res 260:305–308Google Scholar
  64. 64.
    Lee TC, Mohsin S, Taylor D, Parkesh R, Gunnlaugsson T, O’Brien FJ, Giehl M, Gowin W (2003) Detecting microdamage in bone. J Anat 203:161–172Google Scholar
  65. 65.
    Rubin C, Rubin J (2006) Biomechanics and mechanobiology of bone. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism, 6th edn. American Society for Bone and Mineral Research, Washington, pp 36–42Google Scholar
  66. 66.
    Mullender MG, Van der Meer DD, Huisker R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18:109–113Google Scholar
  67. 67.
    Metz LN, Martin RB, Turner AS (2003) Histomorphometric analysis of the effects of osteocyte density on osteonal morphology and remodeling. Bone 33:753–759Google Scholar
  68. 68.
    Bromage TG, Lacruz RS, Hogg R, Goldman HM, McFarlin SC, Warshaw J, Dirks W, Perez-Ochoa A, Smolyar I, Enlow DH, Boyde A (2009) Lamellar bone is an incremental tissue reconciling enamel rhythms, body size, and organismal life history. Calcif Tissue Int 84:388–404Google Scholar
  69. 69.
    Fu H, Fu Q, Zhou N, Huang W, Rahaman MN, Wang D, Liu X (2009) In vitro evaluation of borate-based bioactive glass scaffolds prepared by a polymer foam replication method. Mater Sci Eng C 29:2275–2281Google Scholar
  70. 70.
    Hakki SS, Bozkurt BS, Hakki EE (2010) Boron regulates mineralized tissue-associated proteins in osteoblasts (MC3T3-E1). J Trace Elem Med Biol 24:243–250Google Scholar
  71. 71.
    Ying X, Cheng S, Wang W, Lin Z, Chen Q, Zhang W, Kou D, Shen Y, Cheng X, Rompis FA, Peng L, Zhu Lu C (2011) Effect of boron on osteogenic differentiation of human bone marrow stromal cells. Biol Trace Elem Res 144:306–315Google Scholar
  72. 72.
    Capati ML, Nakazono A, Igawa K, Ookubo K, Yamamoto Y, Yanagiguchi K, Kubo S, Yamada S, Hayashi Y (2016) Boron accelerates cultured osteoblastic cell activity through calcium flux. Biol Trace Elem Res 174:300–308Google Scholar
  73. 73.
    Mori S, Harruff R, Ambrosius W, Burr DB (1997) Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone 21:521–526Google Scholar
  74. 74.
    Robling AG, Turner CH (2002) Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31:562–569Google Scholar
  75. 75.
    Power J, Loveridge N, Rushton N, Parker M, Reeve J (2002) Osteocyte density in aging subjects is enhanced in bone adjacent to remodeling haversian systems. Bone 30:859–865Google Scholar
  76. 76.
    Skedros JG, Hunt KJ, Hughes PE, Winet H (2003) Ontogenetic and regional morphologic variations in the turkey ulna diaphysis: implications for functional adaption of cortical bone. Anat Rec 273A:609–629Google Scholar
  77. 77.
    Skedros JG (2005) Osteocyte lacuna population densities in sheep, elk and horse calcanei. Cells Tissues Organs 181:23–37Google Scholar
  78. 78.
    Hedgecock NL, Hadi T, Chen AA, Curtiss SB, Martin RB, Hazelwood SJ (2007) Quantitative regional associations between remodeling, modeling, and osteocyte apoptosis and density in rabbit tibial midshafts. Bone 40:627–637Google Scholar
  79. 79.
    Schneider P, Stauber M, Voide R, Stampanoni M, Donahue LR, Müller R (2007) Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 22:1557–1570Google Scholar
  80. 80.
    Rizzoli R (2008) Nutrition: its role in bone health. Best Pract Res Clin Endocrinol Metab 22:813–829Google Scholar
  81. 81.
    Lezón CE, Olivera MI, Bozzini C, Mandalunis P, Alippi RM, Boyer PM (2009) Improved bone status by the beta-blocker propranolol in an animal model of nutritional growth retardation. Br J Nutr 101:1616–1620Google Scholar
  82. 82.
    Ferretti JL, Tessaro RD, Delgado CJ, Bozzini CE, Alippi RM, Barceló AC (1988) Biomechanical performance of diaphyseal shafts of bone tissue of femurs from protein-restricted rats. Bone Miner 4:329–339Google Scholar
  83. 83.
    Ferretti JL, Capozza R, Cointry G, Bozzini C, Alippi RM, Bozzini CE (1991) Additive effects of dietary protein and energy deficiencies on diaphysis and bone tissue of rat femurs as determined by bending tests. Acta Physiol Pharmacol Ther Latinoam 41:253–262Google Scholar
  84. 84.
    Boyer PM, Compagnucci GE, Olivera MI, Bozzini C, Roig MC, Compagnucci CV, Alippi RM (2005) Bone status in an animal model of chronic suboptimal nutrition: a morphometric, densitometric and mechanical study. Br J Nutr 93:663–669Google Scholar
  85. 85.
    Fong L, Tan K, Tang C, Cool J, Scherer MA, Elovaris R, Coyle P, Rofe AM, Xian R (2009) Interaction of dietary zinc and intracellular binding metallothionein in postnatal bone growth. Bone 44:1151–1162Google Scholar
  86. 86.
    Chapin RE, Ku WW, Kenney MA, McCoy H, Gladen B, Wine RN, Wilson R, Elwell MR (1997) The effects of dietary boron on bone strength in rats. Fundam Appl Toxicol 35:205–215Google Scholar
  87. 87.
    Chapin RE, Ku WW, Kenney MA, McCoy H (1998) The effect of boron on bone characteristics and plasma lipids in rats. Biol Tarce Elem Res 66:395–399Google Scholar
  88. 88.
    Naghii MR, Tarkaman G, Mofid M (2006) Effects of boron and calcium supplementation on mechanical properties of bone in rats. Biofactors 29:195–201Google Scholar
  89. 89.
    Ferretti JL, Cointry GR, Capozza RF, Frost HM (2003) Bone mass, bone strength, muscle-bone interactions, osteopenias and osteoporoses. Mech Age Dev 124:269–279Google Scholar
  90. 90.
    Callister WD (2007) Materials science and engineering: an introduction. John Wiley & Sons, New YorkGoogle Scholar
  91. 91.
    Blouin S, Thaler HW, Korninger C, Schmid R, Hofstatter JG, Zoehrer R, Phipps R, Klaushofer K, Roschger P, Paschalis EP (2009) Bone matrix quality and plasma homocysteine levels. Bone 44:959–964Google Scholar
  92. 92.
    Nielsen FH (2009) Boron deprivation decreases liver S-adenosylmethionine and spermidine and increases plasma homocysteine and cysteine in rats. J Trace Elem Med Biol 23:204–213Google Scholar
  93. 93.
    Aparicio S, Doty SB, Camacho NP, Paschalis EP, Spevak L, Mendelsohn R, Boskey AL (2002) Optimal methods for processing mineralized tissues for Fourier transform infrared microspectroscopy. Calcif Tissue Int 70:422–429Google Scholar
  94. 94.
    Bachrach LK (2008) Skeletal development in childhood and adolescence. In: Rosen CJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism, 7th edn. American Society for Bone and Mineral Research, Washington, DC, pp 74–79Google Scholar
  95. 95.
    Wang Q, Seeman E (2008) Skeletal growth and peak bone strength. Best Pract Res Clin Endocrinol Metab 22:687–700Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Alejandro A. Gorustovich
    • 1
    Email author
  • Forrest H. Nielsen
    • 2
  1. 1.Interdisciplinary Materials Group-IESIING-UCASALSaltaArgentina
  2. 2.Research Nutritionist ConsultantGrand ForksUSA

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