Silver nanoparticles alter proteoglycan expression in the promotion of tendon repair

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 10, Issue 7, 2014, Pages 1375-1383

  Kwan, Karen H L ^a   Yeung, Kelvin W K ^a,d   Liu, Xuelai ^a   Wong, Kenneth K Y ^a   Shum, Ho Cheung ^b   Lam, Yun Wah ^c   Cheng, Shuk Han ^c   Cheung, Kenneth M C ^a   To, Michael K T ^a,d  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c CITY UNIVERSITY OF HONG KONG   (Hong Kong)

^d THE UNIVERSITY OF HONG KONG SHENZHEN HOSPITAL   (China)

Author keywords

Achilles tendon; Fibromodulin; Healing; Proteoglycan; Silver nanoparticles

Indexed keywords

CELL DEATH; CELL PROLIFERATION; COLLAGEN; HISTOLOGY; METAL NANOPARTICLES; REPAIR; SILVER NANOPARTICLES; SYNTHESIS (CHEMICAL);

ACHILLES TENDONS; CLINICAL APPLICATION; FIBROMODULIN; HEALING; PROLIFERATING CELL NUCLEAR ANTIGENS; PROTEOGLYCAN SYNTHESIS; PROTEOGLYCANS; TUMOR NECROSIS FACTOR ALPHA;

TENDONS;

ANTIINFLAMMATORY AGENT; COLLAGEN; CYCLINE; FIBROMODULIN; PROTEOGLYCAN; SILVER NANOPARTICLE; TUMOR NECROSIS FACTOR ALPHA; WOUND HEALING PROMOTING AGENT; METAL NANOPARTICLE; SILVER;

ACHILLES TENDON; ACHILLES TENDON RUPTURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOMECHANICS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DRUG MECHANISM; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PROTEIN EXPRESSION; PROTEOGLYCAN SYNTHESIS; RAT; TENSILE STRENGTH; TISSUE REGENERATION; WOUND HEALING; ANIMAL; CHEMISTRY; INJURIES; KIDNEY; LIVER; METABOLISM; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TENDON INJURIES;

ACHILLES TENDON; ANIMALS; COLLAGEN; KIDNEY; LIVER; METAL NANOPARTICLES; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; SILVER; TENDON INJURIES;

EID: 84912150701     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2013.11.015     Document Type: Article

References (49)

1. Vailas A.C., Tipton C.M., Laughlin H.L., Tcheng T.K., Matthes R.D. Physical activity and hypophysectomy on the aerobic capacity of ligaments and tendons. J Appl Physiol 1978, 44(4):542-546.
2. Williams J.G. Achilles tendon lesions in sport. Sports Med 1986, 3(2):114-135.
3. Soroceanu A., Sidhwa F., Aarabi S., Kaufman A., Glazebrook M. Surgical versus nonsurgical treatment of acute achilles tendon rupture a meta-analysis of randomized trials. J Bone Joint Surg Am 2012, 94A(23):2136-2143.
4. Jiang N., Wang B.W., Chen A.F., Dong F., Yu B. Operative versus nonoperative treatment for acute Achilles tendon rupture: a meta-analysis based on current evidence. Int Orthop 2012, 36(4):765-773.
5. Kurtz C.A., Loebig T.G., Anderson D.D., DeMeo P.J., Campbell P.G. Insulin-like growth factor I accelerates functional recovery from Achilles tendon injury in a rat model. Am J Sport Med 1999, 27(3):363-369.
6. Heisterbach P.E., Todorov A., Fluckiger R., Evans C.H., Majewski M. Effect of BMP-12, TGF-beta1 and autologous conditioned serum on growth factor expression in Achilles tendon healing. Knee Surg Sports Traumatol Arthrosc 2012, 20(10):1907-1914.
7. Lyras D.N., Kazakos K., Verettas D., et al. The effect of platelet-rich plasma gel in the early phase of patellar tendon healing. Arch Orthop Traum Surg 2009, 129(11):1577-1582.
8. Bolt P., Clerk A.N., Luu H.H., et al. BMP-14 gene therapy increases tendon tensile strength in a rat model of Achilles tendon injury. J Bone Joint Surg Am 2007, 89A(6):1315-1320.
9. Rickert M., Wang H.L., Wieloch P., et al. Adenovirus-mediated gene transfer of growth and differentiation factor-5 into tenocytes and the healing rat Achilles tendon. Connect Tissue Res 2005, 46(4-5):175-183.
10. Majewski M., Betz O., Ochsner P.E., Liu F., Porter R.M., Evans C.H. Ex vivo adenoviral transfer of bone morphogenetic protein 12 (BMP-12) cDNA improves Achilles tendon healing in a rat model. Gene Ther 2008, 15(16):1139-1146.
11. Gulotta L.V., Kovacevic D., Packer J.D., Deng X.H., Rodeo S.A. Bone marrow-derived mesenchymal stem cells transduced with scleraxis improve rotator cuff healing in a rat model. Am J Sports Med 2011, 39(6):1282-1289.
12. Schnabel L.V., Lynch M.E., van der Meulen M.C., Yeager A.E., Kornatowski M.A., Nixon A.J. Mesenchymal stem cells and insulin-like growth factor-I gene-enhanced mesenchymal stem cells improve structural aspects of healing in equine flexor digitorum superficialis tendons. J Orthop Res 2009, 27(10):1392-1398.
13. Longo U.G., Lamberti A., Maffulli N., Denaro V. Tissue engineered biological augmentation for tendon healing: a systematic review. Br Med Bull 2011, 98:31-59.
14. Tian J., Wong K.K., Ho C.M., et al. Topical delivery of silver nanoparticles promotes wound healing. ChemMedChem 2007, 2(1):129-136.
15. Wong K.K.Y., Cheung S.O.F., Huang L.M., et al. Further evidence of the anti-inflammatory effects of silver nanoparticles. ChemMedChem 2009, 4(7):1129-1135.
16. Kwan K.H., Liu X., To M.K., Yeung K.W., Ho C.M., Wong K.K. Modulation of collagen alignment by silver nanoparticles results in better mechanical properties in wound healing. Nanomedicine 2011, 7(4):497-504.
17. Liu X.L., Lee P.Y., Ho C.M., et al. Silver nanoparticles mediate differential responses in keratinocytes and fibroblasts during skin wound healing. Chem Med Chem 2010, 5(3):468-475.
18. Lok C.N., Ho C.M., Chen R., et al. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J Proteome Res 2006, 5(4):916-924.
19. Lopezdeleon A., Rojkind M. A simple micromethod for collagen and total protein determination in formalin-fixed paraffin-embedded sections. J Histochem Cytochem 1985, 33(8):737-743.
20. Ashoka S., Peake B.M., Bremner G., Hageman K.J., Reid M.R. Comparison of digestion methods for ICP-MS determination of trace elements in fish tissues. Anal Chim Acta 2009, 653(2):191-199.
21. Eliasson P., Andersson T., Aspenberg P. Rat Achilles tendon healing: mechanical loading and gene expression. J Appl Physiol 2009, 107(2):399-407.
22. Sharma P., Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskeletal Neuronal Interact 2006, 6(2):181-190.
23. Murphy P.G., Loitz B.J., Frank C.B., Hart D.A. Influence of exogenous growth factors on the synthesis and secretion of collagen types I and III by explants of normal and healing rabbit ligaments. Biochemistry and cell biology =. Biochem Cell Biol 1994, 72(9-10):403-409.
24. Sharma P., Maffulli N. Current concepts review tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am 2005, 87A(1):187-202.
25. Tillman L.J.C.N. Properties of dense connective tissue and wound healing. Management of common musculoskeletal disorders 1996, 8-21. Lippincott, Philadelphia, USA. D. Hertling, R.M. Kessler (Eds.).
26. Hooley C.J., Cohen R.E. Model for the creep-behavior of tendon. Int J Biol Macromol 1979, 1(3):123-132.
27. Foldbjerg R., Olesen P., Hougaard M., Dang D.A., Hoffmann H.J., Autrup H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicol Lett 2009, 190(2):156-162.
28. Hsin Y.H., Chen C.F., Huang S., Shih T.S., Lai P.S., Chueh P.J. The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells (vol 179, pg 130, 2008). Toxicol Lett 2009, 185(2):142.
29. Arora S., Jain J., Rajwade J.M., Paknikar K.M. Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells. Toxicol Appl Pharm 2009, 236(3):310-318.
30. Screen H.R.C., Shelton J.C., Chhaya V.H., Kayser M.V., Bader D.L., Lee D.A. The influence of noncollagenous matrix components on the micromechanical environment of tendon fascicles. Ann Biomed Eng 2005, 33(8):1090-1099.
31. Yoon J.H., Halper J. Tendon proteoglycans: biochemistry and function. J Musculoskelet Neuronal Interact 2005, 5(1):22-34.
32. Jepsen K.J., Wu F., Peragallo J.H., et al. A syndrome of joint laxity and impaired tendon integrity in lumican- and fibromodulin-deficient mice. J Biol Chem 2002, 277(38):35532-35540.
33. Gelberman R.H., Manske P.R., Vande Berg J.S., Lesker P.A., Akeson W.H. Flexor tendon repair in vitro: a comparative histologic study of the rabbit, chicken, dog, and monkey. J Orthop Res 1984, 2(1):39-48.
34. Riedererhenderson M.A., Gauger A., Olson L., Robertson C., Greenlee T.K. Attachment and extracellular-matrix differences between tendon and synovial fibroblastic cells. In Vitro Cell Dev B 1983, 19(2):127-133.
35. Fujita M., Hukuda S., Doida Y. Experimental study of intrinsic healing of the flexor tendon: collagen synthesis of the cultured flexor tendon cells of the canine. Nihon Seikeigeka Gakkai Zasshi 1992, 66(4):326-333.
36. Mori R., Shaw T.J., Martin P. Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring. J Exp Med 2008, 205(1):43-51.
37. Stramer B.M., Mori R., Martin P. The inflammation-fibrosis link? A Jekyll and Hyde role for blood cells during wound repair. J Invest Dermatol 2007, 127(5):1009-1017.
38. Ashcroft G.S., Yang X., Glick A.B., et al. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1999, 1(5):260-266.
39. Martin P., D'Souza D., Martin J., et al. Wound healing in the PU.1 null mouse-tissue repair is not dependent on inflammatory cells. Curr Biol 2003, 13(13):1122-1128.
40. John T., Lodka D., Kohl B., et al. Effect of pro-inflammatory and immunoregulatory cytokines on human tenocytes. J Orthop Res 2010, 28(8):1071-1077.
41. Rees S.G., Dent C.M., Caterson B. Metabolism of proteoglycans in tendon. Scand J Med Sci Sports 2009, 19(4):470-478.
42. Hosaka Y., Kirisawa R., Ueda H., Yamaguchi M., Takehana K. Differences in tumor necrosis factor (TNF)alpha and TNF receptor-1-mediated intracellular signaling factors in normal, inflamed and scar-formed horse tendons. J Vet Med Sci 2005, 67(10):985-991.
43. Lankveld D.P.K., Oomen A.G., Krystek P., et al. The kinetics of the tissue distribution of silver nanoparticles of different sizes. Biomaterials 2010, 31(32):8350-8361.
44. Dziendzikowska K., Gromadzka-Ostrowska J., Lankoff A., et al. Time-dependent biodistribution and excretion of silver nanoparticles in male Wistar rats. J Appl Toxicol 2012, 32(11):920-928.
45. Kim Y.S., Kim J.S., Cho H.S., et al. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhal Toxicol 2008, 20(6):575-583.
46. Rahman M.F., Wang J., Patterson T.A., et al. Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol Lett 2009, 187(1):15-21.
47. Ji J.H., Jung J.H., Kim S.S., et al. Twenty-eight-day inhalation toxicity study of silver nanoparticles in Sprague-Dawley rats. Inhal Toxicol 2007, 19(10):857-871.
48. Hyun J.S., Lee B.S., Ryu H.Y., Sung J.H., Chung K.H., Yu I.J. Effects of repeated silver nanoparticles exposure on the histological structure and mucins of nasal respiratory mucosa in rats. Toxicol Lett 2008, 182(1-3):24-28.
49. Takenaka S., Karg E., Roth C., et al. Pulmonary and systemic distribution of inhaled ultrafine silver particles in rats. Environ Health Perspect 2001, 109:547-551.