Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
Current Osteoporosis Reports
Published in: Current Osteoporosis Reports 2/2015

Open Access 01-04-2015 | Osteocytes (T Bellido and J Klein-Nulend, Section Editors)

Osteocyte Shape and Mechanical Loading

Authors: René F. M. van Oers, Hong Wang, Rommel G. Bacabac

Published in: Current Osteoporosis Reports | Issue 2/2015

Login to get access

Abstract

There is considerable variation in the shape of osteocyte lacunae, which is likely to influence the function of osteocytes as the professional mechanosensors of bone. In this review, we first discussed how mechanical loading could affect the shape of osteocyte lacunae. Recent studies show that osteocyte lacunae are aligned to collagen. Since collagen fiber orientation is affected by loading mode, this alignment may help to understand how mechanical loading shapes the osteocyte lacuna. Secondly, we discussed how the shape of osteocytes could influence their mechanosensation. In vitro, round osteocytes are more mechanosensitive than flat osteocytes. Altered lacunar morphology has been associated with bone pathology. It is important to know whether osteocyte shape is part of the etiology.
Literature
1.
Cowin SC, Moss-Salentijn L, Moss ML. Candidates for the mechanosensory system in bone. J Biomech Eng. 1991;113:191–7.CrossRefPubMed
2.
Mullender MG, Huiskes R. Proposal for the regulatory mechanism of Wolff’s law. J Orthop Res. 1995;13:503–12.CrossRefPubMed
3.
Burger EH, Klein-Nulend J. Mechanotransduction in bone—role of the lacuno-canalicular network. FASEB J. 1999;13(Suppl):S101–12.PubMed
4.
Cowin SC. The significance of bone microstructure in mechanotransduction. J Biomech. 2007;40(Suppl):S105–9.CrossRefPubMed
5.
Bonivtch AR, Bonewald LF, Nicolella DP. Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J Biomech. 2007;40:2199–206.CrossRefPubMedCentralPubMed
6.
Pazzaglia UE, Congiu T. The cast imaging of the osteon lacunar-canalicular system and the implications with functional models of intracanalicular flow. J Anat. 2013;222(2):193–202.CrossRefPubMedCentralPubMed
7.
Wang Y, McNamara LM, Schaffler MB, Weinbaum S. A model for the role of integrins in flow induced mechanotransduction in osteocytes. Proc Natl Acad Sci U S A. 2007;104:15941–6.CrossRefPubMedCentralPubMed
8.
McNamara LM, Majeska RJ, Weinbaum S, Friedrich V, Schaffler MB. Attachment of osteocyte cell processes to the bone matrix. Anat Rec (Hoboken). 2009;292:355–63.CrossRef
9.
Nicolella DP, Nicholls AE, Lankford J, Davy DT. Machine vision photogrammetry: a technique for measurement of microstructural strain in cortical bone. J Biomech. 2001;34:135–9.CrossRefPubMed
10.
Fukada E, Yasuda I. On the piezoelectric effect of bone. J Phys Soc Jpn. 1957;12:1158–62.CrossRef
11.
Salzstein RA, Pollack SR, Mak AF, Petrov N. Electromechanical potentials in cortical bone—I. A continuum approach. J Biomech. 1987;20:261–70.CrossRefPubMed
12.
Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. 1994;27:339–60.CrossRefPubMed
13.
Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S. Mechanosensation and transduction in osteocytes. Bone. 2013;54:182–90.CrossRefPubMed
14.
Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EH. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts—correlation with prostaglandin upregulation. Biochem Biophys Res Commun. 1995;217:640–8.CrossRefPubMed
15.
Ajubi NE, Klein-Nulend J, Nijweide PJ, Vrijheid-Lammers T, Alblas MJ, Burger EH. Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes—a cytoskeleton dependent process. Biochem Biophys Res Commun. 1996;225:62–8.CrossRefPubMed
16.
Han Y, Cowin SC, Schaffler MB, Weinbaum S. Mechanotransduction and strain amplification in osteocyte cell processes. Proc Natl Acad Sci U S A. 2004;101:16689–94.CrossRefPubMedCentralPubMed
17.
You L, Cowin SC, Schaffler MB, Weinbaum S. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech. 2001;34:1375–86.CrossRefPubMed
18.
Kamioka H, Kameo Y, Imai Y, Bakker AD, Bacabac RG, Yamada N, et al. Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model. Integr Biol. 2012;4:1198–206.CrossRef
19.
Marotti G, Muglia MA, Zaffe D. A SEM study of osteocyte orientation in alternately structured osteons. Bone. 1985;6:331–4.CrossRefPubMed
20.
Rensberger JM, Watabe M. Fine structure of bone in dinosaurs, birds and mammals. Nature. 2000;406:619–22.CrossRefPubMed
21.
Marotti G. Osteocyte orientation in human lamellar bone and its relevance to the morphometry of periosteocytic lacunae. Metab Bone Dis Rel Res. 1979;1:325–33.CrossRef
22.
D’Emic MD, Benson RB. Measurement, variation, and scaling of osteocyte lacunae: a case study in birds. Bone. 2013;57:300–10.CrossRefPubMed
23.
Dong P, Haupert S, Hesse B, Langer M, Gouttenoire PJ, Bousson V, et al. 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone. 2014;60:172–85.CrossRefPubMed
24.
Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J. Osteocyte morphology in fibula and calvaria—is there a role for mechanosensing? Bone. 2008;43:452–8.CrossRefPubMed
25.
Teti A, Zallone A. Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone. 2009;44:11–6.CrossRefPubMed
26.
27.
Zallone A, Teti A, Primavera MV, Pace G. Mature osteocytes behavior in a repletion period: the occurrence of osteoplastic activity. Bas Appl Histochem. 1983;27:191–204.
28.••
Kerschnitzki M, Wagermaier W, Roschger P, Seto J, Shahar R, Duda GN, et al. The organization of the osteocyte network mirrors the extracellular matrix orientation in bone. J Struct Biol. 2011;173:303–11. Demonstrates a correlation between lacunar orientation and collagen fiber orientation. CrossRefPubMed
29.
Jones SJ, Boyde A. Is there a relationship between osteoblasts and collagen orientation in bone? Isr J Med Sci. 1976;12:98–107.PubMed
30.•
Matsugaki A, Isobe Y, Saku T, Nakano T. Quantitative regulation of bone-mimetic, oriented collagen/apatite matrix structure depends on the degree of osteoblast alignment on oriented collagen substrates. J Biomed Mater Res A. 2014. Shows osteoblast alignment to collagen substrate in vitro.
31.
Misof K, Landis WJ, Klaushofer K, Fratzl P. Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. J Clin Invest. 1997;100:40–5.CrossRefPubMedCentralPubMed
32.
Thomopoulos S, Marquez JP, Weinberger B, Birman V, Genin GM. Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations. J Biomech. 2006;39:1842–51.CrossRefPubMed
33.
Bromage TG, Goldman HM, McFarlin SC, Warshaw J, Boyde A, Riggs CM. Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat Rec B New Anat. 2003;274(1):157–68.CrossRefPubMed
34.
McMahon JM, Boyde A, Bromage TG. Pattern of collagen fiber orientation in the ovine calcaneal shaft and its relation to locomotor-induced strain. Anat Rec. 1995;242:147–58.CrossRefPubMed
35.•
Skedros JG, Keenan KE, Williams TJ, Kiser CJ. Secondary osteon size and collagen/lamellar organization (“osteon morphotypes”) are not coupled, but potentially adapt independently for local strain mode or magnitude. J Struct Biol. 2013;181:95–107. Investigates osteon morphotypes in relation to loading mode. CrossRefPubMed
36.
Petrtyl M, Hert J, Fiala P. Spatial organization of the Haversian bone in man. J Biomech. 1996;29:161–9.CrossRefPubMed
37.
Smit TH, Burger EH. Is BMU-coupling a strain-regulated phenomenon? A finite element analysis. J Bone Miner Res. 2000;15:301–7.CrossRefPubMed
38.
Smit TH, Burger EH, Huyghe JM. A case for strain-induced fluid flow as a regulator of BMU-coupling and osteonal alignment. J Bone Miner Res. 2002;17:2021–9.CrossRefPubMed
39.
van Oers RFM, Ruimerman R, Tanck E, Hilbers PAJ, Huiskes R. A unified theory for osteonal and hemi-osteonal remodeling. Bone. 2008;42:250–9.CrossRefPubMed
40.
van Oers RFM, Ruimerman R, van Rietbergen B, Hilbers PAJ, Huiskes R. Relating osteon diameter to strain. Bone. 2008;43:476–82.CrossRefPubMed
41.
Wilson W, Driessen NJ, van Donkelaar CC, Ito K. Prediction of collagen orientation in articular cartilage by a collagen remodeling algorithm. Osteoarthritis Cartilage. 2006;14:1196–202.CrossRefPubMed
42.
Driessen NJ, Wilson W, Bouten CV, Baaijens FP. A computational model for collagen fibre remodelling in the arterial wall. J Theor Biol. 2004;226:53–64.CrossRefPubMed
43.
Flynn BP, Bhole AP, Saeidi N, Liles M, DiMarzio CA, Ruberti JW. Mechanical strain stabilizes reconstituted collagen fibrils against enzymatic degradation by mammalian collagenase matrix metalloproteinase 8 (MMP-8). PLoS One. 2010;5:e12337.CrossRefPubMedCentralPubMed
44.
Curtze S, Dembo M, Miron M, Jones DB. Dynamic changes in traction forces with DC electric field in osteoblast-like cells. J Cell Sci. 2004;117:2721–9.CrossRefPubMed
45.
Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res. 2000;15:60–7.CrossRefPubMed
46.
Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodeling in response to in vivo fatigue microdamage. J Biomech. 1985;18:189–200.CrossRefPubMed
47.
Prendergast PJ, Huiskes R. Microdamage and osteocyte-lacuna strain in bone: a microstructural finite element analysis. J Biomech Eng. 1996;118:240–6.CrossRefPubMed
48.
Bacabac RG, Mizuno D, Schmidt CF, MacKintosh FC, Van Loon JJ, Klein-Nulend J, et al. Round versus flat: bone cell morphology, elasticity, and mechanosensing. J Biomech. 2008;41:1590–8.CrossRefPubMed
49.
Qiu J, Baik AD, Lu XL, Hillman EM, Zhuang Z, Dong C, et al. A noninvasive approach to determine viscoelastic properties of an individual adherent cell under fluid flow. J Biomech. 2014;47:1537–41.CrossRefPubMed
50.
van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, Smit TH, et al. Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density—is there a role for mechanosensing? Bone. 2009;45:321–9.CrossRefPubMed
51.
McCreadie BR, Hollister SJ, Schaffler MB, Goldstein SA. Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech. 2004;37:563–72.CrossRefPubMed
52.
Mullender MG, Dijcks SJ, Bacabac RG, Semeins CM, Van Loon JJ, Klein-Nulend J. Release of nitric oxide, but not prostaglandin E2, by bone cells depends on fluid flow frequency. J Orthop Res. 2006;24:1170–7.CrossRefPubMed
53.
Bacabac RG, Van Loon JJ, Smit TH, Klein-Nulend J. Noise enhances the rapid nitric oxide production by bone cells in response to fluid shear stress. Technol Health Care. 2009;17:57–65.PubMed
Metadata
Title
Osteocyte Shape and Mechanical Loading
Authors
René F. M. van Oers
Hong Wang
Rommel G. Bacabac
Publication date
01-04-2015
Publisher
Springer US
Published in
Current Osteoporosis Reports / Issue 2/2015
Print ISSN: 1544-1873
Electronic ISSN: 1544-2241
DOI
https://doi.org/10.1007/s11914-015-0256-1

Other articles of this Issue 2/2015

Current Osteoporosis Reports 2/2015 Go to the issue

Nutrition, Exercise, and Lifestyle in Osteoporosis (CM Weaver and R Daly, Section Editors)

Diet, Gut Microbiome, and Bone Health

Bone and Diabetes (AV Schwartz and P Vestergaard, Section Editors)

Diabetes, Diabetic Complications, and Fracture Risk

Osteocytes (T Bellido and J Klein-Nulend, Section Editors)

Cx43 and Mechanotransduction in Bone

Skeletal Development (E Schanipani and E Zelzer, Section Editors)

The Immunological Contribution to Heterotopic Ossification Disorders

Rare Bone Disease (CB Langman and E Shore, Section Editors)

Hypophosphatemic Rickets: Lessons from Disrupted FGF23 Control of Phosphorus Homeostasis

Rare Bone Disease (CB Langman and E Shore, Section Editors)

Hyperphosphatemic Familial Tumoral Calcinosis: Genetic Models of Deficient FGF23 Action