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Published in: BMC Musculoskeletal Disorders 1/2015

Open Access 01-12-2015 | Research article

Hyaluronic acid increases tendon derived cell viability and collagen type I expression in vitro: Comparative study of four different Hyaluronic acid preparations by molecular weight

Authors: Leonardo Osti, Martina Berardocco, Viviana di Giacomo, Graziella Di Bernardo, Francesco Oliva, Anna C. Berardi

Published in: BMC Musculoskeletal Disorders | Issue 1/2015

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Abstract

Background

Hyaluronic Acid (HA) has been already approved by Food and Drug Administration (FDA) for osteoarthritis (OA), while its use in the treatment of tendinopathy is still debated. The aim of this study was to evaluate in human rotator cuff tendon derived cells the effects of four different HA on cell viability, proliferation, apoptosis and the expression of collagen type I and collagen type III.

Methods

An in vitro model was developed on human tendon derived cells from rotator cuff tears to study the effects of four different HA preparations (Ps) (sodium hyaluronate MW: 500-730 KDa - Hyalgan®, 1000 kDa Artrosulfur HA®, 1600 KDa Hyalubrix® and 2200 KDa Synolis-VA®) at various concentrations. Tendon derived cells morphology were evaluated after 0, 7 and 14 d of culture. Viability, proliferation, apoptosis were evaluated after 0, 24 and 48 h of culture. The expression and deposition of collagen type I and collagen type III were evaluated after 1, 7 and 14 d of culture.

Results

All HAPs tested increased viability and proliferation, in dose dependent manner. HAPs already reduce apoptosis at 24 h compared to control cells (without HAPs). Furthermore, HAPs stimulated the synthesis of collagen type I in a dose dependent fashion over 14 d, without increase in collagen type III; moreover, in the presence of Synolis-VA® the expression and deposition of collagen type I was significantly higher as compare with the other HAPs.

Conclusions

HAPs enhanced viability, proliferation and expression of collagen type I in tendon derived cells.
Literature
1.
go back to reference Oliva F, Osti L, Padulo J, Maffulli N. Epidemiology of the rotator cuff tears: a new incidence related to thyroid disease. Muscles Ligaments Tendons J. 2014;4(3):309–14.PubMedPubMedCentral Oliva F, Osti L, Padulo J, Maffulli N. Epidemiology of the rotator cuff tears: a new incidence related to thyroid disease. Muscles Ligaments Tendons J. 2014;4(3):309–14.PubMedPubMedCentral
2.
go back to reference Osti L, Rizzello G, Panascì M, Denaro V, Maffulli N. Full thickness tears: retaining the cuff. Sports Med Arthosc. 2011;19(4):409–19.CrossRef Osti L, Rizzello G, Panascì M, Denaro V, Maffulli N. Full thickness tears: retaining the cuff. Sports Med Arthosc. 2011;19(4):409–19.CrossRef
3.
go back to reference Oliva F, Berardi AC, Misiti S, Maffulli N. Thyroid hormones and tendon: current views and future perspectives. Concise review. Muscles Ligaments Tendons J. 2013;3(3):201–3.PubMedPubMedCentral Oliva F, Berardi AC, Misiti S, Maffulli N. Thyroid hormones and tendon: current views and future perspectives. Concise review. Muscles Ligaments Tendons J. 2013;3(3):201–3.PubMedPubMedCentral
4.
go back to reference Klatte-Schulz F, Pauly S, Scheibel M, Greiner S, Gerhardt C, Schmidmaier G, et al. Influence of age on the cell biological characteristics and the stimulation potential of male human tenocyte-like cells. Eur Cell Mater. 2012;24:74–89.PubMed Klatte-Schulz F, Pauly S, Scheibel M, Greiner S, Gerhardt C, Schmidmaier G, et al. Influence of age on the cell biological characteristics and the stimulation potential of male human tenocyte-like cells. Eur Cell Mater. 2012;24:74–89.PubMed
5.
go back to reference Loppini M, Maffulli N. Conservative management of tendinopathy: an evidence-based approach. Muscles Ligaments Tendons J. 2012;1(4):134–7.PubMedPubMedCentral Loppini M, Maffulli N. Conservative management of tendinopathy: an evidence-based approach. Muscles Ligaments Tendons J. 2012;1(4):134–7.PubMedPubMedCentral
6.
go back to reference Rutjes AW, Jüni P, da Costa BR, Trelle S, Nüesch E, Reichenbach S. Viscosupplementation for osteoarthitis of the knee: a systematic review and meta-analysis. Ann Intern Med. 2012;157(3):180–91.CrossRefPubMed Rutjes AW, Jüni P, da Costa BR, Trelle S, Nüesch E, Reichenbach S. Viscosupplementation for osteoarthitis of the knee: a systematic review and meta-analysis. Ann Intern Med. 2012;157(3):180–91.CrossRefPubMed
8.
go back to reference Giai Via A, De Cupis M, Spoliti M, Oliva F. Clinical and biological aspects of rotator cuff tears. Muscles Ligaments Tendons J. 2014;3(4):359. Giai Via A, De Cupis M, Spoliti M, Oliva F. Clinical and biological aspects of rotator cuff tears. Muscles Ligaments Tendons J. 2014;3(4):359.
9.
10.
go back to reference Benson RT, McDonnell SM, Knowles HJ, Rees JL, Carr AJ, Hulley PA. Tendinopathy and tears of the rotator cuff are associated with hypoxia and apoptosis. J Bone Joint Surg Br. 2010;92(3):448–53.CrossRefPubMedPubMedCentral Benson RT, McDonnell SM, Knowles HJ, Rees JL, Carr AJ, Hulley PA. Tendinopathy and tears of the rotator cuff are associated with hypoxia and apoptosis. J Bone Joint Surg Br. 2010;92(3):448–53.CrossRefPubMedPubMedCentral
11.
go back to reference Meyer K. Chemical structure of hyaluronic acid. Fed Proc. 1958;17(4):1075–7.PubMed Meyer K. Chemical structure of hyaluronic acid. Fed Proc. 1958;17(4):1075–7.PubMed
12.
go back to reference Melrose J, Numata Y, Ghosh P. Biotinylated hyaluronan: a versatile and highly sensitive probe capable of detecting nanogram levels of hyaluronan binding proteins (hyaladherins) on electroblots by a novel affinity detection procedure. Electrophoresis. 1996;17(1):205.CrossRefPubMed Melrose J, Numata Y, Ghosh P. Biotinylated hyaluronan: a versatile and highly sensitive probe capable of detecting nanogram levels of hyaluronan binding proteins (hyaladherins) on electroblots by a novel affinity detection procedure. Electrophoresis. 1996;17(1):205.CrossRefPubMed
13.
go back to reference Chen WY, Grant ME, Schor AM, Schor SL. Differences between adult and fetal fibroblasts in the regulation of hyaluronate synthesis: correlation with migratory activity. J Cell Sci. 1989;94(Pt 3):577–84.PubMed Chen WY, Grant ME, Schor AM, Schor SL. Differences between adult and fetal fibroblasts in the regulation of hyaluronate synthesis: correlation with migratory activity. J Cell Sci. 1989;94(Pt 3):577–84.PubMed
14.
go back to reference Klein ES, Asculai SS, Ben-Ari GY. Effects of hyaluronic acid on fibroblast behavior in peritoneal injury. J Surg Res. 1996;61(2):473–6.CrossRefPubMed Klein ES, Asculai SS, Ben-Ari GY. Effects of hyaluronic acid on fibroblast behavior in peritoneal injury. J Surg Res. 1996;61(2):473–6.CrossRefPubMed
15.
go back to reference Hall CL, Wang C, Lange LA, Turley EA. Hyaluronan and the hyaluronan receptor RHAMM promote focal adhesion turnover and transient tyrosine kinase activity. J Cell Biol. 1994;126(2):575–88.CrossRefPubMed Hall CL, Wang C, Lange LA, Turley EA. Hyaluronan and the hyaluronan receptor RHAMM promote focal adhesion turnover and transient tyrosine kinase activity. J Cell Biol. 1994;126(2):575–88.CrossRefPubMed
16.
go back to reference Wiig M, Abrahamsson SO, Lundborg G. Effects of hyaluronan on cell proliferation and collagen synthesis: a study of rabbit flexor tendons in vitro. J Hand Surg Am. 1996;21(4):599–604. Wiig M, Abrahamsson SO, Lundborg G. Effects of hyaluronan on cell proliferation and collagen synthesis: a study of rabbit flexor tendons in vitro. J Hand Surg Am. 1996;21(4):599–604.
17.
go back to reference Bernard E, Hornebeck W, Robert L. Effect of hyaluronan on the elastase-type activity of human skin fibroblasts. Cell Biol Int. 1994;18(10):967–71.CrossRefPubMed Bernard E, Hornebeck W, Robert L. Effect of hyaluronan on the elastase-type activity of human skin fibroblasts. Cell Biol Int. 1994;18(10):967–71.CrossRefPubMed
18.
go back to reference Matuoka K, Namba M, Mitsui Y. Hyaluronate synthetase inhibition by normal and transformed human fibroblasts during growth reduction. J Cell Biol. 1987;104(4):1105–15.CrossRefPubMed Matuoka K, Namba M, Mitsui Y. Hyaluronate synthetase inhibition by normal and transformed human fibroblasts during growth reduction. J Cell Biol. 1987;104(4):1105–15.CrossRefPubMed
19.
go back to reference Dean BJ, Snelling SJ, Dakin SG, Murphy RJ, Javaid MK, Carr AJ. Differences in glutamate receptors and inflammatory cell numbers are associated with the resolution of pain in human rotator cuff tendinopathy. Arthritis Res Ther. 2015;17:176.CrossRefPubMedPubMedCentral Dean BJ, Snelling SJ, Dakin SG, Murphy RJ, Javaid MK, Carr AJ. Differences in glutamate receptors and inflammatory cell numbers are associated with the resolution of pain in human rotator cuff tendinopathy. Arthritis Res Ther. 2015;17:176.CrossRefPubMedPubMedCentral
20.
go back to reference Oliva F, Berardi AC, Misiti S, Verga Falzacappa C, Iacone A, Maffulli N. Thyroid hormones enhance growth and counteract apoptosis in human tenocytes isolated from rotator cuff tendons. Cell Death Disease. 2013;4:e705.CrossRefPubMedPubMedCentral Oliva F, Berardi AC, Misiti S, Verga Falzacappa C, Iacone A, Maffulli N. Thyroid hormones enhance growth and counteract apoptosis in human tenocytes isolated from rotator cuff tendons. Cell Death Disease. 2013;4:e705.CrossRefPubMedPubMedCentral
21.
go back to reference Yao L, Bestwick CS, Bestwick LA, Maffulli N, Aspden RM. Phenotypic drift in human tenocyte culture. Tissue Eng. 2006;12(7):1843–9.CrossRefPubMed Yao L, Bestwick CS, Bestwick LA, Maffulli N, Aspden RM. Phenotypic drift in human tenocyte culture. Tissue Eng. 2006;12(7):1843–9.CrossRefPubMed
22.
go back to reference Yuan J, Murrell GA, Trickett A, Wang MX. Involvement of cytochome c release and caspase-3 activation in the oxidative stress-induced apoptosis in human tendon fibroblasts. Biochimica et Biophysica Acta. 2003;1641(1):35–41.CrossRefPubMed Yuan J, Murrell GA, Trickett A, Wang MX. Involvement of cytochome c release and caspase-3 activation in the oxidative stress-induced apoptosis in human tendon fibroblasts. Biochimica et Biophysica Acta. 2003;1641(1):35–41.CrossRefPubMed
23.
go back to reference Berardi AC, Oliva F, Berardocco M, la Rovere M, Accorsi P, Maffulli N. Thyroid hormones increase collagen type Iand cartilage oligomeric matrix protein (COMP) expression in vitro human tenocytes. Muscles Ligaments Tendons J. 2014;4(3):285–91.PubMedPubMedCentral Berardi AC, Oliva F, Berardocco M, la Rovere M, Accorsi P, Maffulli N. Thyroid hormones increase collagen type Iand cartilage oligomeric matrix protein (COMP) expression in vitro human tenocytes. Muscles Ligaments Tendons J. 2014;4(3):285–91.PubMedPubMedCentral
24.
go back to reference Hanna S, Khalil B, Nasrallah A, Saykali BA, Sobh R, Nasser S, et al. StarD13 is a tumor suppressor in breast cancer that regulates cell motility and invasion. Int J Oncol. 2014;44(5):1499–511.PubMedPubMedCentral Hanna S, Khalil B, Nasrallah A, Saykali BA, Sobh R, Nasser S, et al. StarD13 is a tumor suppressor in breast cancer that regulates cell motility and invasion. Int J Oncol. 2014;44(5):1499–511.PubMedPubMedCentral
26.
go back to reference Karna E, Miltyk W, Surazyński A, Pałka JA. Protective effect of hyaluronic acid on interleukin-1-induced deregulation of beta1-integrin and insulin-like growth factor-I receptor signaling and collagen biosynthesis in cultured human chondrocytes. Mol Cell Biochem. 2008;308(1–2):57–64.CrossRefPubMed Karna E, Miltyk W, Surazyński A, Pałka JA. Protective effect of hyaluronic acid on interleukin-1-induced deregulation of beta1-integrin and insulin-like growth factor-I receptor signaling and collagen biosynthesis in cultured human chondrocytes. Mol Cell Biochem. 2008;308(1–2):57–64.CrossRefPubMed
27.
go back to reference Oliva F, Gatti S, Porcellini G, Forsyth NR, Maffulli N. Growth factors and tendon healing. Med Sport Sci. 2012;57:53–64.CrossRefPubMed Oliva F, Gatti S, Porcellini G, Forsyth NR, Maffulli N. Growth factors and tendon healing. Med Sport Sci. 2012;57:53–64.CrossRefPubMed
28.
go back to reference Maffulli N, Ewen SW, Waterston SW, Reaper J, Barrass V. Tenocytes from ruptured and tendinopathic achilles tendons produce greater quantities of type III collagen than tenocytes from normal achilles tendons. An in vitro model of human tendon healing. Am J Sports Med. 2000;28(4):499–505.PubMed Maffulli N, Ewen SW, Waterston SW, Reaper J, Barrass V. Tenocytes from ruptured and tendinopathic achilles tendons produce greater quantities of type III collagen than tenocytes from normal achilles tendons. An in vitro model of human tendon healing. Am J Sports Med. 2000;28(4):499–505.PubMed
29.
go back to reference Yamada T, Gotoh M, Nakama K, Mitsui Y, Higuchi F, Nagata K. Effects of hyaluronan on cell proliferation and mRNA expression of procollagens alpha 1 (I) and alpha 1 (III) in tendon-derived fibroblasts from patients with rotator cuff disease: an in vitro study. Am J Sports Med. 2007;35(11):1870–6.CrossRefPubMed Yamada T, Gotoh M, Nakama K, Mitsui Y, Higuchi F, Nagata K. Effects of hyaluronan on cell proliferation and mRNA expression of procollagens alpha 1 (I) and alpha 1 (III) in tendon-derived fibroblasts from patients with rotator cuff disease: an in vitro study. Am J Sports Med. 2007;35(11):1870–6.CrossRefPubMed
Metadata
Title
Hyaluronic acid increases tendon derived cell viability and collagen type I expression in vitro: Comparative study of four different Hyaluronic acid preparations by molecular weight
Authors
Leonardo Osti
Martina Berardocco
Viviana di Giacomo
Graziella Di Bernardo
Francesco Oliva
Anna C. Berardi
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2015
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-015-0735-7

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