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Comparison of tissue transglutaminase 2 and bone biological markers osteocalcin, osteopontin and sclerostin expression in human osteoporosis and osteoarthritis

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Abstract

Osteoporosis (OP) and osteoarthritis (OA) are the most common joint diseases, with a high incidence in the elderly population. OP is characterized by trabecular bone remodeling and reabsorption, whereas articular cartilage and subchondral bone remodeling are major features of OA. Although classically considered as independent or even conflicting processes, clinical coexistence of OP and OA was recently described. Transglutaminase 2 (TG2) expression is considered a biomarker of OA, but its role in osteoporotic bone remodeling is still uncertain. We investigated TG2 and bone biological markers (Osteocalcin, Osteopontin, and Sclerostin) in osteoporotic and osteoarthritic osteocartilagineous tissue (n = 54) and human chondrocyte cultures in vitro by immunohistochemistry, immunofluorescence and RT-PCR. Histomorphometric evaluation of bone trabecular remodeling was also performed. In cartilage, TG2 expression was faint in control and OP and significantly less than in OA and OP + OA chondrocytes; the opposite was found for Osteocalcin, whereas Osteopontin and Sclerostin expression was similar. In the subchondral trabecular bone, osteocytes/osteoblasts TG2 expression was slight and similar comparing control, OP, OA, and OP + OA group, whereas Osteocalcin and Osteopontin expression was lower in OP compared to control, OA and OP + OA. Increased TG2 and reduced Osteocalcin expression were maintained in human osteoarthritic chondrocytes in vitro. Histomorphometric analysis confirmed reduced trabecular bone mass in OP and OP + OA compared with OA patients. TG2 represented a suitable biomarker of osteoarthritic chondrocyte activation, whereas osteocalcin and osteopontin characterized osteoporotic osteocyte/osteoblast changes; differences were lost in OP + OA patients, suggesting careful consideration when coexistence of the two diseases occurs.

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References

  • Ardawi MS, Al-Kadi HA, Rouzi AA, Qari MH (2011) Determinants of serum sclerostin in healthy pre- and postmenopausal women. J Bone Miner Res 26:2812–2822. doi:10.1002/jbmr.479

    Article  CAS  PubMed  Google Scholar 

  • Arden NK, Crozier S, Smith H, Anderson F, Edwards C, Raphael H, Cooper C (2006) Knee pain, knee osteoarthritis, and the risk of fracture. Arthritis Rheum 55:610–615. doi:10.1002/art.22088

    Article  PubMed  Google Scholar 

  • Bei R, Budillon A, Masuelli L, Cereda V, Vitolo D, Di Gennaro E, Ripavecchia V, Palumbo C, Ionna F, Losito S, Modesti A, Kraus MH, Muraro R (2004) Frequent overexpression of multiple ErbB receptors by head and neck squamous cell carcinoma contrasts with rare antibody immunity in patients. J Pathol 204:317–325. doi:10.1002/path.1642

    Article  CAS  PubMed  Google Scholar 

  • Beil FT, Seitz S, Priemel M, Barvencik F, von Domarus C, Rueger JM, Amling M, Pogoda P (2008) Pathophysiology and pathomorphology of osteoporosis. Eur J Trauma Emerg Surg 34:527–534. doi:10.1007/s00068-008-8201-y

    Article  PubMed  Google Scholar 

  • Beninati S, Senger DR, Cordella-Miele E, Mukherjee AB, Chackalaparampil I, Shanmugam V, Singh K, Mukherjee BB (1994) Osteopontin: its transglutaminase-catalyzed posttranslational modifications and cross-linking to fibronectin. J Biochem 115:675–682

    Article  CAS  PubMed  Google Scholar 

  • Bergink AP, van der Klift M, Hofman A, Verhaar JA, van Leeuwen JP, Uitterlinden AG, Pols HA (2003) Osteoarthritis of the knee is associated with vertebral and nonvertebral fractures in the elderly: the Rotterdam Study. Arthritis Rheum 49:648–657. doi:10.1002/art.11380

    Article  PubMed  Google Scholar 

  • Berry PA, Maciewicz RA, Cicuttini FM, Jones MD, Hellawell CJ, Wluka AE (2010) Markers of bone formation and resorption identify subgroups of patients with clinical knee osteoarthritis who have reduced rates of cartilage loss. J Rheumatol 37:1252–1259. doi:10.3899/jrheum.091055

    Article  CAS  PubMed  Google Scholar 

  • Bhadada SK, Rastogi A, Steenackers E, Boudin E, Arya A, Dhiman V, Bhansali A, Van Hul W (2013) Novel SOST gene mutation in a sclerosteosis patient and her parents. Bone 52:707–710. doi:10.1016/j.bone.2012.10.009

    Article  CAS  PubMed  Google Scholar 

  • Cassinelli G, Zuco V, Petrangolini G, De Cesare M, Tortoreto M, Lanzi C, Cominetti D, Zaffaroni N, Orlandi A, Passeri D, Meco D, Di Francesco AM, Riccardi R, Bucci F, Pisano C, Zunino F (2012) The curative efficacy of namitecan (ST1968) in preclinical models of pediatric sarcoma is associated with antiangiogenic effects. Biochem Pharmacol 84:163–171. doi:10.1016/j.bcp.2012.04.005

    Article  CAS  PubMed  Google Scholar 

  • Cervelli V, Scioli MG, Gentile P, Doldo E, Bonanno E, Spagnoli LG, Orlandi A (2012) Platelet-rich plasma greatly potentiates insulin-induced adipogenic differentiation of human adipose-derived stem cells through a serine/threonine kinase Akt-dependent mechanism and promotes clinical fat graft maintenance. Stem Cells Transl Med 1:206–220. doi:10.5966/sctm.2011-0052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan BY, Fuller ES, Russell AK, Smith SM, Smith MM, Jackson MT, Cake MA, Read RA, Bateman JF, Sambrook PN, Little CB (2011) Increased chondrocyte sclerostin may protect against cartilage degradation in osteoarthritis. Osteoarthr Cartil 19:874–885. doi:10.1016/j.joca.2011.04.014

    Article  CAS  PubMed  Google Scholar 

  • Chang IC, Chiang TI, Yeh KT, Lee H, Cheng YW (2010) Increased serum osteopontin is a risk factor for osteoporosis in menopausal women. Osteoporos Int 21:1401–1409. doi:10.1007/s00198-009-1107-7

    Article  CAS  PubMed  Google Scholar 

  • Chen JS, Mehta K (1999) Tissue transglutaminase: an enzyme with a split personality. Int J Biochem Cell Biol 31:817–836. doi:10.1016/S1357-2725(99)00045-X

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Bal BS, Gorski JP (1992) Calcium and collagen binding properties of osteopontin, bone sialoprotein, and bone acidic glycoprotein-75 from bone. J Biol Chem 267:24871–24878

    CAS  PubMed  Google Scholar 

  • Collins DH, McElligotte TF (1960) Sulphate (35SO4) uptake by chondrocytes in relation to histological changes in osteoarthritic human articular cartilage. Ann Rheum Dis 19:318–330. doi:10.1136/ard.19.4.318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cumming RG, Klineberg RJ (1993) Epidemiological study of the relation between arthritis of the hip and hip fractures. Ann Rheum Dis 52:707–710. doi:10.1136/ard.52.10.717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR, Parfitt AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 28:2–17. doi:10.1002/jbmr.1805

    Article  PubMed  PubMed Central  Google Scholar 

  • Denhardt DT, Noda M (1998) Osteopontin expression and function: role in bone remodeling. J Cell Biochem Suppl 30–31:92–102. doi:10.1002/(SICI)1097-4644(1998)72:30/31+92:AID-JCB13>3.0.CO;2-A

    Article  PubMed  Google Scholar 

  • Dequeker J, Johnell O (1993) Osteoarthritis protects against femoral neck fracture: the MEDOS study experience. Bone 14(Suppl 1):S51–S56. doi:10.1186/1471-2474-11-274

    Article  PubMed  Google Scholar 

  • Dieppe PA, Lohmander LS (2005) Pathogenesis and management of pain in osteoarthritis. Lancet 365:965–973. doi:10.1016/S0140-6736(05)71086-2

    Article  CAS  PubMed  Google Scholar 

  • Eastell R, Hannon RA (2008) Biomarkers of bone health and osteoporosis risk. Proc Nutr Soc 67:157–162. doi:10.1017/S002966510800699X

    Article  PubMed  Google Scholar 

  • Felson DT (2009) Developments in the clinical understanding of osteoarthritis. Arthritis Res Ther 11:203. doi:10.1186/ar2531

    Article  PubMed  PubMed Central  Google Scholar 

  • Fesus L, Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27:534–539. doi:10.1016/S0968-0004(02)02182-5

    Article  CAS  PubMed  Google Scholar 

  • Funck-Brentano T, Cohen-Solal M (2011) Crosstalk between cartilage and bone: when bone cytokines matter. Cytokine Growth Factor Rev 22:91–97. doi:10.1016/j.cytogfr.2011.04.003

    Article  CAS  PubMed  Google Scholar 

  • Gao SG, Li KH, Zeng KB, Tu M, Xu M, Lei GH (2010) Elevated osteopontin level of synovial fluid and articular cartilage is associated with disease severity in knee osteoarthritis patients. Osteoarthr Cartil 18:82–87. doi:10.1016/j.joca.2009.07.009

    Article  CAS  PubMed  Google Scholar 

  • Goldring MB, Goldring SR (2010) Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Ann N Y Acad Sci 1192:230–237. doi:10.1111/j.1749-632.2009.05240.x

    Article  CAS  PubMed  Google Scholar 

  • Harris WH (1969) Traumatic arthritis of the hip after dislocation and acetabular fractures: treatment by mold arthroplasty. An end-result study using a new method of result evaluation. J Bone Jt Surg Am 51:737–755

    Article  CAS  Google Scholar 

  • Heath DJ, Downes S, Verderio E, Griffin M (2001) Characterization of tissue transglutaminase in human osteoblast-like cells. J Bone Miner Res 16:1477–1485. doi:10.1359/jbmr.2001.16.8.1477

    Article  CAS  PubMed  Google Scholar 

  • Heiland GR, Zwerina K, Baum W, Kireva T, Distler JH, Grisanti M, Asuncion F, Li X, Ominsky M, Richards W, Schett G, Zwerina J (2010) Neutralisation of Dkk-1 protects from systemic bone loss during inflammation and reduces sclerostin expression. Ann Rheum Dis 69:2152–2159. doi:10.1136/ard.2010.132852

    Article  CAS  PubMed  Google Scholar 

  • Hinton R, Moody RL, Davis A, Thomas S (2002) Osteoarthritis: diagnosis and therapeutic considerations. Am Fam Physician 65:841–848

    PubMed  Google Scholar 

  • Jakob M, Démarteau O, Schäfer D, Stumm M, Heberer M, Martin I (2003) Enzymatic digestion of adult human articular cartilage yields a small fraction of the total available cells. Connect Tissue Res 44:173–180

    Article  CAS  PubMed  Google Scholar 

  • Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17:1726–1733. doi:10.1007/s00198-006-0172-4

    Article  CAS  PubMed  Google Scholar 

  • Johnson VL, Hunter DJ (2014) The epidemiology of osteoarthritis. Best Pract Res Clin Rheumatol 28:5–15. doi:10.1016/j.berh.2014.01.004

    Article  PubMed  Google Scholar 

  • Johnson K, Hashimoto S, Lotz M, Pritzker K, Terkeltaub R (2001) Interleukin-1 induces pro-mineralizing activity of cartilage tissue transglutaminase and factor XIIIa. Am J Pathol 159:149–163. doi:10.1016/S0002-9440(10)61682-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaartinen MT, Pirhonen A, Linnala-Kankkunen A, Mäenpää PH (1997) Transglutaminase-catalyzed cross-linking of osteopontin is inhibited by osteocalcin. J Biol Chem 272:22736–22741. doi:10.1074/jbc.272.36.22736

    Article  CAS  PubMed  Google Scholar 

  • Kaartinen MT, El-Maadawy S, Räsänen NH, McKee MD (2002) Tissue transglutaminase and its substrates in bone. J Bone Miner Res 17:2161–2173. doi:10.1359/jbmr.2002.17.12.2161

    Article  CAS  PubMed  Google Scholar 

  • Karsdal MA, Leeming DJ, Dam EB, Henriksen K, Alexandersen P, Pastoureau P, Altman RD, Christiansen C (2008) Should subchondral bone turnover be targeted when treating osteoarthritis? Osteoarthr Cartil 16:638–646. doi:10.1016/j.joca.2008.01.014

    Article  CAS  PubMed  Google Scholar 

  • Krause C, Korchynskyi O, de Rooij K, Weidauer SE, de Gorter DJ, van Bezooijen RL, Hatsell S, Economides AN, Mueller TD, Löwik CW, ten Dijke P (2010) Distinct modes of inhibition by sclerostin on bone morphogenetic protein and Wnt signaling pathways. J Biol Chem 285:41614–41626. doi:10.1074/jbc.M110.153890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuliwaba JS, Findlay DM, Atkins GJ, Forwood MR, Fazzalari NL (2000) Enhanced expression of osteocalcin mRNA in human osteoarthritic trabecular bone of the proximal femur is associated with decreased expression of interleukin-6 and interleukin-11 mRNA. J Bone Miner Res 15:332–341. doi:10.1359/jbmr.2000.15.2.332

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zhang H, Yang C, Li Y, Dai Z (2016) An overview of osteocalcin progress. J Bone Miner Metab. doi:10.1007/s00774-015-0734-7

    Google Scholar 

  • Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4:140–156. doi:10.1038/nrm1014

    Article  CAS  PubMed  Google Scholar 

  • Manenti G, Capuani S, Fanucci E, Assako EP, Masala S, Sorge R, Iundusi R, Tarantino U, Simonetti G (2013) Diffusion tensor imaging and magnetic resonance spectroscopy assessment of cancellous bone quality in femoral neck of healthy, osteopenic and osteoporotic subjects at 3T: preliminary experience. Bone 55:7–15. doi:10.1016/j.bone.2013.03.004

    Article  PubMed  Google Scholar 

  • Matsui Y, Iwasaki N, Kon S, Takahashi D, Morimoto J, Matsui Y, Denhardt DT, Rittling S, Minami A, Uede T (2009) Accelerated development of aging-associated and instability-induced osteoarthritis in osteopontin-deficient mice. Arthritis Rheum 60:2362–2371. doi:10.1002/art.24705

    Article  CAS  PubMed  Google Scholar 

  • McKee MD, Glimcher MJ, Nanci A (1992) High-resolution immunolocalization of osteopontin and osteocalcin in bone and cartilage during endochondral ossification in the chicken tibia. Anat Rec 234:479–492. doi:10.1002/ar.1092340404

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee BB, Nemir M, Beninati S, Cordella-Miele E, Singh K, Chackalaparampil I, Shanmugam V, DeVouge MW, Mukherjee AB (1995) Interaction of osteopontin with fibronectin and other extracellular matrix molecules. Ann N Y Acad Sci 760:201–212. doi:10.1111/j.1749-6632.1995.tb44631.x

    Article  CAS  PubMed  Google Scholar 

  • Nilsdotter A, Bremander A (2011) Measures of hip function and symptoms: Harris Hip Score (HHS), Hip Disability and Osteoarthritis Outcome Score (HOOS), Oxford Hip Score (OHS), Lequesne Index of Severity for Osteoarthritis of the Hip (LISOH), and American Academy of Orthopedic Surgeons (AAOS) Hip and Knee Questionnaire. Arthritis Care Res (Hoboken) 63(Suppl 11):S200–S207. doi:10.1002/acr.20549

    Article  Google Scholar 

  • Orlandi A, Ferlosio A, Ciucci A, Sesti F, Lifschitz-Mercer B, Gabbiani G, Spagnoli LG, Czernobilsky B (2004) Cellular retinol-binding protein-1 expression in endometrial stromal cells: physiopathological and diagnostic implications. Histopathology 45:511–517. doi:10.1111/j.1365-2559.2004.01963.x

    Article  CAS  PubMed  Google Scholar 

  • Orlandi A, Ciucci A, Ferlosio A, Pellegrino A, Chiariello L, Spagnoli LG (2005) Increased expression and activity of matrix metalloproteinases characterize embolic cardiac myxomas. Am J Pathol 166:1619–1628. doi:10.1016/S0002-9440(10)62472-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orlandi A, Oliva F, Taurisano G, Candi E, Di Lascio A, Melino G, Spagnoli LG, Tarantino U (2009) Transglutaminase-2 differently regulates cartilage destruction and osteophyte formation in a surgical model of osteoarthritis. Amino Acids 36:755–763. doi:10.1007/s00726-008-0129-3

    Article  CAS  PubMed  Google Scholar 

  • Piters E, Culha C, Moester M, Van Bezooijen R, Adriaensen D, Mueller T, Weidauer S, Jennes K, de Freitas F, Löwik C, Timmermans JP, Van Hul W, Papapoulos S (2010) First missense mutation in the SOST gene causing sclerosteosis by loss of sclerostin function. Hum Mutat 31:E1526–E1543. doi:10.1002/humu.21274

    Article  CAS  PubMed  Google Scholar 

  • Power J, Poole KE, van Bezooijen R, Doube M, Caballero-Alías AM, Lowik C, Papapoulos S, Reeve J, Loveridge N (2010) Sclerostin and the regulation of bone formation: effects in hip osteoarthritis and femoral neck fracture. J Bone Miner Res 25:1867–1876. doi:10.1002/jbmr.70

    Article  CAS  PubMed  Google Scholar 

  • Pullig O, Weseloh G, Gauer S, Swoboda B (2000a) Osteopontin is expressed by adult human osteoarthritic chondrocytes: protein and mRNA analysis of normal and osteoarthritic cartilage. Matrix Biol 19:245–255. doi:10.1016/S0945-053X(00)00068-8

    Article  CAS  PubMed  Google Scholar 

  • Pullig O, Weseloh G, Ronneberger D, Käkönen S, Swoboda B (2000b) Chondrocyte differentiation in human osteoarthritis: expression of osteocalcin in normal and osteoarthritic cartilage and bone. Calcif Tissue Int 67:230–240. doi:10.1007/s002230001108

    Article  CAS  PubMed  Google Scholar 

  • Ravaud P, Ayral X, Dougados M (1999) Radiologic progression of hip and knee osteoarthritis. Osteoarthr Cartil 7:222–229. doi:10.1007/s10067-015-3146-0

    Article  CAS  PubMed  Google Scholar 

  • Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Harris SE, Turner CH (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283:5866–5875. doi:10.1074/jbc.M705092200

    Article  CAS  PubMed  Google Scholar 

  • Rosenthal AK, Derfus BA, Henry LA (1997) Transglutaminase activity in aging articular chondrocytes and articular cartilage vesicles. Arthritis Rheum 40:966–970. doi:10.1002/art.1780400526

    Article  CAS  PubMed  Google Scholar 

  • Roudier M, Li X, Niu QT, Pacheco E, Pretorius JK, Graham K, Yoon BR, Gong J, Warmington K, Ke HZ, Black RA, Hulme J, Babij P (2013) Sclerostin is expressed in articular cartilage but loss or inhibition does not affect cartilage remodeling during aging or following mechanical injury. Arthritis Rheum 65:721–731. doi:10.1002/art.37802

    Article  CAS  PubMed  Google Scholar 

  • Ryan LM, McCarty DJ (1997) Calcium pyrophosphate crystal deposition disease, pseudogout, and articular condrocalcinosis. In: Koopman W (ed) Arthritis and allied conditions: a textbook of rheumatology, 13th edn. Williams and Wilkins, Baltimore, pp 2103–2126

    Google Scholar 

  • Sanchez C, Deberg MA, Bellahcène A, Castronovo V, Msika P, Delcour JP, Crielaard JM, Henrotin YE (2008) Phenotypic characterization of osteoblasts from the sclerotic zones of osteoarthritic subchondral bone. Arthritis Rheum 58:442–455. doi:10.1002/art.23159

    Article  CAS  PubMed  Google Scholar 

  • Sarahrudi K, Thomas A, Albrecht C, Aharinejad S (2012) Strongly enhanced levels of sclerostin during human fracture healing. J Orthop Res 30:1549–1555. doi:10.1002/jor.22129

    Article  CAS  PubMed  Google Scholar 

  • Semënov M, Tamai K, He X (2005) SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J Biol Chem 280:26770–26775. doi:10.1074/jbc.M504308200

    Article  PubMed  Google Scholar 

  • Spagnoli LG, Orlandi A, Marino B, Mauriello A, De Angelis C, Ramacci MT (1995) Propionyl-l-carnitine prevents the progression of atherosclerotic lesions in aged hyperlipemic rabbits. Atherosclerosis 114:29–44. doi:10.1016/0021-9150(94)05460-Z

    Article  CAS  PubMed  Google Scholar 

  • Standal T, Borset M, Sundan A (2004) Role of osteopontin in adhesion, migration, cell survival and bone remodeling. Exp Oncol 26:179–184

    CAS  PubMed  Google Scholar 

  • Summey BT Jr, Graff RD, Lai TS, Greenberg CS, Lee GM (2002) Tissue transglutaminase localization and activity regulation in the extracellular matrix of articular cartilage. J Orthop Res 20:76–82. doi:10.1016/S0736-0266(01)00064-X

    Article  CAS  PubMed  Google Scholar 

  • Tarantino U, Ferlosio A, Arcuri G, Spagnoli LG, Orlandi A (2013) Transglutaminase 2 as a biomarker of osteoarthritis: an update. Amino Acids 44:199–207. doi:10.1007/s00726-011-1181-y

    Article  CAS  PubMed  Google Scholar 

  • Tarantino U, Celi M, Rao C, Feola M, Cerocchi I, Gasbarra E, Ferlosio A, Orlandi A (2014) Hip osteoarthritis and osteoporosis: clinical and histomorphometric considerations. Int J Endocrinol 2014:372021. doi:10.1155/2014/372021

    Article  PubMed  PubMed Central  Google Scholar 

  • Thomázy VA, Davies PJ (1999) Expression of tissue transglutaminase in the developing chicken limb is associated both with apoptosis and endochondral ossification. Cell Death Differ 6:146–154

    Article  PubMed  Google Scholar 

  • Vestergaard P, Rejnmark L, Mosekilde L (2009) Osteoarthritis and risk of fractures. Calcif Tissue Int 84:249–256. doi:10.1007/s00223-009-9224-z

    Article  CAS  PubMed  Google Scholar 

  • Wanby P, Nobin R, Von SP, Brudin L, Carlsson M (2016) Serum levels of the bone turnover markers dickkopf-1, sclerostin, osteoprotegerin, osteopontin, osteocalcin and 25-hydroxyvitamin D in Swedish geriatric patients aged 75 years or older with a fresh hip fracture and in healthy controls. J Endocrinol Invest. doi:10.1007/s40618-015-0421-5

    PubMed  Google Scholar 

  • WHO (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organ Tech Rep Ser 843:1–129

    Google Scholar 

  • Winkler DG, Sutherland MK, Geoghegan JC, Yu C, Hayes T, Skonier JE, Shpektor D, Jonas M, Kovacevich BR, Staehling-Hampton K, Appleby M, Brunkow ME, Latham JA (2003) Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J 22:6267–6276. doi:10.1093/emboj/cdg599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wozniak M, Fausto A, Carron CP, Meyer DM, Hruska KA (2000) Mechanically strained cells of the osteoblast lineage organize their extracellular matrix through unique sites of alphavbeta3-integrin expression. J Bone Miner Res 15:1731–1745. doi:10.1359/jbmr.2000.15.9.1731

    Article  CAS  PubMed  Google Scholar 

  • Wright NC, Lisse JR, Walitt BT, Eaton CB, Chen Z (2011) Arthritis increases the risk for fractures–results from the Women’s Health Initiative. J Rheumatol 38:1680–1688. doi:10.3899/jrheum.101196

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang ZM, Li ZC, Jiang LS, Jiang SD, Dai LY (2010) Micro-CT and mechanical evaluation of subchondral trabecular bone structure between postmenopausal women with osteoarthritis and osteoporosis. Osteoporos Int 21:1383–1390. doi:10.1007/s00198-009-1071-2

    Article  PubMed  Google Scholar 

  • Zoch ML, Clemens TL, Riddle RC (2016) New insights into the biology of osteocalcin. Bone 82:42–49. doi:10.1016/j.bone.2015.05.046

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors acknowledge ASI (Italian Space Agency) and University of Rome “Tor Vergata” (Spatial Biomedicine Center) for partially founding this study (number search DC-DTE-2011-033). Thanks to S. Cappelli for technical assistance and to M. Feola and C. Rao for collection of clinical data.

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    1. Anatomic Pathology, Department of Biomedicine and Prevention, Tor Vergata University of Rome, Rome, Italy

      Chiara Tarquini, Francesca Mastrangeli, Sara Agostinelli, Amedeo Ferlosio & Augusto Orlandi

    2. General Pathology, Department of Clinical Sciences and Translational Medicine, Tor Vergata University of Rome, Rome, Italy

      Rosanna Mattera & Roberto Bei

    3. Department of Orthopedics and Traumatology, Tor Vergata University of Rome, Rome, Italy

      Chiara Tarquini, Francesca Mastrangeli & Umberto Tarantino

    4. Policlinic of Tor Vergata of Rome, Rome, Italy

      Augusto Orlandi & Umberto Tarantino

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    1. Chiara Tarquini
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    All procedures performed in this study involving human participants were in accordance with the ethical standards of the University of “Tor Vergata”, Ethic Committees and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study. This article does not contain any studies with animals performed by any of the authors.

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    C. Tarquini and R. Mattera contributed equally to the paper. A. Orlandi and U. Tarantino contributed equally to the paper.

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    Tarquini, C., Mattera, R., Mastrangeli, F. et al. Comparison of tissue transglutaminase 2 and bone biological markers osteocalcin, osteopontin and sclerostin expression in human osteoporosis and osteoarthritis. Amino Acids 49, 683–693 (2017). https://doi.org/10.1007/s00726-016-2290-4

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