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08.03.2018 | Original Article

Can photobiomodulation associated with implantation of mesenchymal adipose-derived stem cells attenuate the expression of MMPs and decrease degradation of type II collagen in an experimental model of osteoarthritis?

verfasst von: Tatiane Garcia Stancker, Stella Souza Vieira, Andrey Jorge Serra, Rafael do Nascimento Lima, Regiane dos Santos Feliciano, José Antônio Silva Jr., Solange Almeida dos Santos, Marcia Ataize dos Santos Vieira, Maíra Cecília Brandão Simões, Ernesto Cesar Leal-Junior, Paulo de Tarso Camillo de Carvalho

Erschienen in: Lasers in Medical Science | Ausgabe 5/2018

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Abstract

This study aimed to determine whether photobiomodulation therapy (PBMT) could improve the bioavailability and chondroprotective benefits of mesenchymal stem cells injected into the knees of rats used as an experimental model of osteoarthritis (OA) as well as reduce the expression of matrix metalloproteinases (MMPs) and degradation of type II collagen (COL2-1) in the cartilage. Adipose-derived stem/stromal cells (ADSCs) were collected from three male Fischer 344 rats and characterized by flow cytometry. Fifty female Fischer 344 rats were distributed into five groups of 10 animals each. These groups were as follows: control, OA, OA PBMT, OA ADSC, and OA ADSC PBMT. OA was induced in the animals using a 4% papain solution. Animals from the OA ADSC and OA ADSC PBMT groups received an intra-articular injection of 10 × 10⁶ ADSCs and were treated with PBMT by irradiation (wavelength: 808 nm, power: 50 mW, energy: 42 J, energy density: 71.2 J/cm², spot size: 0.028). Euthanasia was performed 7 days after the first treatment. The use of PBMT alone and the injection of ADSCs resulted in downregulation of pro-inflammatory cytokines and MPs in cartilage compared to the OA group. PBMT and ADSCs caused upregulation of tissue inhibitors of MPs 1 and 2 and mRNA and protein expression of COL2-1 in cartilage compared to the OA group. The intra-articular injection of ADSCs and PBMT prevented joint degeneration resulting from COL2-1 degradation and modulated inflammation by downregulating cytokines and MMPs in the OA group.

Haque Bhuyan MZ, Tamura Y, Sone E, Yoshinari Y, Maeda C, Takahashi M et al (2017) The intra-articular injection of RANKL-binding peptides inhibits cartilage degeneration in a murine model of osteoarthritis. J Pharmacol Sci:S1347–S8613. https://doi.org/10.1016/j.jphs.2017.05.008

Mardones R, Jofré CM, Tobar L, Minguell JJ (2017) Mesenchymal stem cell therapy in the treatment of hip osteoarthritis. J Hip Preserv Surg 4(2):159–163. https://doi.org/10.1093/jhps/hnx011 CrossRefPubMedPubMedCentral

Fernandes JC, Martel-Pelletier J, Pelletier JP (2002) The role of cytokines in osteoarthritis pathophysiology. Biorheology 39(1–2):237–246PubMed

Wehling N, Palmer GD, Pilapil C, Liu F, Wells JW, Müller PE, … Porter RM (2009). Interleukin-1 and tumor necrosis factor-α inhibit chondrogenesis by human mesenchymal stem cells through NF-κB dependent pathways. Arthritis Rheum 60(3):801–812. doi:https://doi.org/10.1002/art.24352

Kapoor M, Martel-Pelletier J, Lajeunesse D, Pelletier JP, Fahmi H (2011) Role of proinflammatory cytokines in the pathophysiology of osteoarthritis. Nat Rev Rheumatol 7(1):33–42. https://doi.org/10.1038/nrrheum.2010.196 CrossRefPubMed

Clark IM, Swingler TE, Sampieri CL, Edwards DR (2008) The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol 40(6–7):1362–1378. https://doi.org/10.1016/j.biocel.2007.12.006 CrossRefPubMed

Zhu Y, Wang Y, Zhao B, Niu X, Hu B, Li Q et al (2017) Comparison of exosomes secreted by induced pluripotent stem cell-derived mesenchymal stem cells and synovial membrane-derived mesenchymal stem cells for the treatment of osteoarthritis. Stem Cell Res Ther 8(1):64. https://doi.org/10.1186/s13287-017-0510-9 CrossRefPubMedPubMedCentral

Alves ACA, Vieira R d P, Leal-Junior ECP, dos Santos SA, Ligeiro AP, Albertini R et al (2013) Effect of low-level laser therapy on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Arthritis Res Ther 15(5):R116. https://doi.org/10.1186/ar4296 CrossRefPubMedPubMedCentral

Bora P, Majumdar AS (2017) Adipose tissue-derived stromal vascular fraction in regenerative medicine: a brief review on biology and translation. Stem Cell Res Ther 8(1):145. https://doi.org/10.1186/s13287-017-0598-y CrossRefPubMedPubMedCentral

10.

Bansal H, Comella K, Leon J, Verma P, Agrawal D, Koka P et al (2017) Intra-articular injection in the knee of adipose derived stromal cells (stromal vascular fraction) and platelet rich plasma for osteoarthritis. J Transl Med 15(1):141. https://doi.org/10.1186/s12967-017-1242-4 CrossRefPubMedPubMedCentral

11.

Pelttari K, Steck E, Richter W (2008) The use of mesenchymal stem cells for chondrogenesis. Injury 39(1):S58–S65. https://doi.org/10.1016/j.injury.2008.01.038 CrossRefPubMed

12.

Steck E, Fischer J, Lorenz H, Gotterbarm T, Jung M, Richter W (2009) Mesenchymal stem cell differentiation in an experimental cartilage defect: restriction of hypertrophy to bone-close neocartilage. Stem Cells Dev 18(7):969–978. https://doi.org/10.1089/scd.2008.0213 CrossRefPubMed

13.

Agrawal T, Gupta GK, Rai V, Carroll JD, Hamblin MR (2014) Pre-conditioning with low-level laser (light) therapy: light before the storm. Dose Response 12(4):619–649. https://doi.org/10.2203/dose-response.14-032 CrossRefPubMedPubMedCentral

14.

Marcos RL, Leal-Junior EC, Arnold G, Magnenet V, Rahouadj R, Wang X, Demeurie F, Magdalou J, de Carvalho MH, Lopes-Martins RÁ (2012) Low-level laser therapy in collagenase-induced Achilles tendinitis in rats: analyses of biochemical and biomechanical aspects. J Orthop Res 30(12):1945–1951. https://doi.org/10.1002/jor.22156 CrossRefPubMed

15.

Marcos RL, Leal Junior EC, Messias Fde M, de Carvalho MH, Pallotta RC, Frigo L, dos Santos RA, Ramos L, Teixeira S, Bjordal JM, Lopes-Martins RÁ (2011) Infrared (810 nm) low-level laser therapy in rat Achilles tendinitis: a consistent alternative to drugs. Photochem Photobiol 87(6):1447–1452. https://doi.org/10.1111/j.1751-1097.2011.00999.x CrossRefPubMed

16.

Laraia EM, Silva IS, Pereira DM, dos Reis FA, Albertini R, de Almeida P, Leal Junior EC, de Tarso Camillo de Carvalho P (2012) Effect of low-level laser therapy (660 nm) on acute inflammation induced by tenotomy of Achilles tendon in rats. Photochem Photobiol 88(6):1546–1550. https://doi.org/10.1111/j.1751-1097.2012.01179.x CrossRefPubMed

17.

Tomazoni SS, Frigo L, Dos Reis Ferreira TC, Casalechi HL, Teixeira S, de Almeida P, Muscara MN, Marcos RL, Serra AJ, de Carvalho PTC, Leal-Junior ECP (2017) Effects of photobiomodulation therapy and topical non-steroidal anti-inflammatory drug on skeletal muscle injury induced by contusion in rats-part 1: morphological and functional aspects. Lasers Med Sci 32(9):2111–2120. https://doi.org/10.1007/s10103-017-2346-z CrossRefPubMed

18.

Tomazoni SS, Frigo L, Dos Reis Ferreira TC, Casalechi HL, Teixeira S, de Almeida P, Muscara MN, Marcos RL, Serra AJ, de Carvalho PTC, Leal-Junior ECP (2017) Effects of photobiomodulation therapy and topical non-steroidal anti-inflammatory drug on skeletal muscle injury induced by contusion in rats-part 2: biochemical aspects. Lasers Med Sci 32(8):1879–1887. https://doi.org/10.1007/s10103-017-2299-2 CrossRefPubMed

19.

Kushibiki T, Hirasawa T, Okawa S, Ishihara M (2015) Low reactive level laser therapy for mesenchymal stromal cells therapies. Stem Cells Int 974864. doi:https://doi.org/10.1155/2015/974864

20.

de Oliveira TS, Serra AJ, Manchini MT, Bassaneze V, Krieger JE, de Tarso Camillo de Carvalho P et al (2015) Effects of low level laser therapy on attachment, proliferation, and gene expression of VEGF and VEGF receptor 2 of adipocyte-derived mesenchymal stem cells cultivated under nutritional deficiency. Lasers Med Sci 30:217–223CrossRefPubMed

21.

Tuby H, Maltz L, Oron U (2007) Low-level laser irradiation (LLLI) promotes proliferation of mesenchymal and cardiac stem cells in culture. Lasers Surg Med 39:373–378CrossRefPubMed

22.

Bassaneze V, Barauna VG, Lavini-Ramos C et al (2010) Shear stress induces nitric oxide-mediates vascular endothelial growth factor production in human adipose tissue mesenchymal stem cells. Stem Cells Dev 19:371–378CrossRefPubMed

23.

da Rosa AS, dos Santos AF, da Silva MM, Facco GG, Perreira DM, Alves ACA et al (2012) Effects of low-level laser therapy at wavelengths of 660 and 808 nm in experimental model of osteoarthritis. Photochem Photobiol 88:161–166. https://doi.org/10.1111/j.1751-1097.2011.01032.x CrossRefPubMed

24.

Mei L, Shen B, Ling P, Liu S, Xue J, Liu F et al (2017) Culture-expanded allogenic adipose tissue-derived stem cells attenuate cartilage degeneration in an experimental rat osteoarthritis model. PLoS One 12(4):e0176107. https://doi.org/10.1371/journal.pone.0176107 CrossRefPubMedPubMedCentral

25.

Benito MJ, Veale DJ, FitzGerald O, van den Berg WB, Bresnihan B (2005) Synovial tissue inflammation in early and late osteoarthritis. Ann Rheum Dis 64(9):1263–1267CrossRefPubMedPubMedCentral

26.

Mazor M, Cesaro A, Ali M, Best TM, Lespessaille E, Toumi H (2017) Progenitor cells from cartilage: grade specific differences in stem cell marker expression. Int J Mol Sci 18(8):E1759. https://doi.org/10.3390/ijms18081759 CrossRefPubMed

27.

Alves AC, Albertini R, dos Santos SA, Leal-Junior EC, Santana E, Serra AJ et al (2014) Effect of low-level laser therapy on metalloproteinase MMP-2 and MMP-9 production and percentage of collagen types I and III in a papain cartilage injury model. Lasers Med Sci 29(3):911–919. https://doi.org/10.1007/s10103-013-1427-x PubMedCrossRef

28.

dos Santos SA, Alves AC, Leal-Junior EC, Albertini R, Vieira RP, Ligeiro AP et al (2014) Comparative analysis of two low-level laser doses on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Lasers Med Sci 29(3):1051–1058. https://doi.org/10.1007/s10103-013-1467-2 PubMedCrossRef

29.

Wang M, Shen J, Jin H, Im HJ, Sandy J, Chen D (2011) Recent progress in understanding molecular mechanisms of cartilage degeneration during osteoarthritis. Ann N Y Acad Sci 1240:61–69. https://doi.org/10.1111/j.1749-6632.2011.06258.x CrossRefPubMedPubMedCentral

30.

Platas J, Guillén MI, del Caz MD, Gomar F, Mirabet V, Alcaraz MJ (2013) Conditioned media from adipose tissue derived mesenchymal stem cells downregulate degradative mediators induced by interleukin-1β in osteoarthritic chondrocytes. Mediat Inflamm 2013:357014. https://doi.org/10.1155/2013/357014 CrossRef

31.

van Buul GM, Villafuertes E, Bos PK, Waarsing JH, Kops N, Narcisi R et al (2012) Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteoarthritic synovium and cartilage explant culture. Osteoarthr Cartil 20(10):1186–1196. https://doi.org/10.1016/j.joca.2012.06.003 CrossRefPubMed

32.

Freemont AJ, Hampson V, Tilman R, Goupille P, Taiwo Y, Hoyland JA (1997) Gene expression of matrix metalloproteinases 1, 3, and 9 by chondrocytes in osteoarthritic human knee articular cartilage is zone and grade specific. Ann Rheum Dis 56(9):542–549CrossRefPubMedPubMedCentral

33.

Tong W, Geng Y, Huang Y, Shi Y, Xiang S, Zhang N et al (2015) In vivo identification and induction of articular cartilage stem cells by inhibiting NF-κB signaling in osteoarthritis. Stem Cells 33(10):3125–3137. https://doi.org/10.1002/stem.2124 CrossRefPubMed

34.

Liu J, Khalil RA (2017) Matrix metalloproteinase inhibitors as investigational and therapeutic tools in unrestrained tissue remodeling and pathological disorders. Prog Mol Biol Transl Sci 148:355–420. https://doi.org/10.1016/bs.pmbts.2017.04.003 CrossRefPubMedPubMedCentral

35.

Wang J, Ma J, Gu JH, Wang FY, Shang XS, Tao HR et al (2017) Regulation of type II collagen, matrix metalloproteinase-13 and cell proliferation by interleukin-1β is mediated by curcumin via inhibition of NF-κB signaling in rat chondrocytes. Mol Med Rep 16(2):1837–1845. https://doi.org/10.3892/mmr.2017.6771 CrossRefPubMedPubMedCentral

36.

Desando G, Cavallo C, Sartoni F, Martini L, Parrilli A, Veronesi F et al (2013) Intra-articular delivery of adipose derived stromal cells attenuates osteoarthritis progression in an experimental rabbit model. Arthritis Res Ther 15(1):R22. https://doi.org/10.1186/ar4156 CrossRefPubMedPubMedCentral

37.

Jin R, Shen M, Yu L, Wang X, Lin X (2017) Adipose-derived stem cells suppress inflammation induced by IL-1β through down-regulation of P2X7R mediated by miR-373 in chondrocytes of osteoarthritis. Molecules and Cells 40(3):222–229. https://doi.org/10.14348/molcells.2017.2314 PubMedPubMedCentralCrossRef

38.

Goldring SR, Goldring MB (2004) The role of cytokines in cartilage matrix degeneration in osteoarthritis. Clin Orthop Relat Res 427:S27–S36CrossRef

39.

Farley J, Dejica VC, Mort JS (2012) Proteases and cartilage degradation in osteoarthritis. Principles of osteoarthritis—its definition, character, derivation and modality-related recognition. Dr. Bruce M. Rothschild (Ed.), InTech

40.

Goldring MB (2012) Articular cartilage degradation in osteoarthritis. HSS J 8(1):7–9. https://doi.org/10.1007/s11420-011-9250-z CrossRefPubMedPubMedCentral

41.

Dejica VM, Mort JS, Laverty S, Antoniou J, Zukor DJ, Tanzer M et al (2012) Increased type II collagen cleavage by cathepsin K and collagenase activities with aging and osteoarthritis in human articular cartilage. Arthritis Res Ther 14(3):R113. https://doi.org/10.1186/ar3839 CrossRefPubMedPubMedCentral

42.

Kuroda K, Kabata T, Hayashi K, Maeda T, Kajino Y, Iwai S et al (2015) The paracrine effect of adipose-derived stem cells inhibits osteoarthritis progression. BMC Musculoskelet Disord 16:236. https://doi.org/10.1186/s12891-015-0701-4 CrossRefPubMedPubMedCentral

43.

ter Huurne M, Schelbergen R, Blattes R, Blom A, de Munter W, Grevers LC et al (2012) Antiinflammatory and chondroprotective effects of intraarticular injection of adipose-derived stem cells in experimental osteoarthritis. Arthritis Rheum 64:3604–3613. https://doi.org/10.1002/art.34626 CrossRefPubMed

44.

Behrendt P, Preusse-Prange A, Klüter T, Haake M, Rolauffs B, Grodzinsky AJ, Lippross S, Kurz B (2016) IL-10 reduces apoptosis and extracellular matrix degradation after injurious compression of mature articular cartilage. Osteoarthr Cartil 24(11):1981–1988. https://doi.org/10.1016/j.joca.2016.06.016 CrossRefPubMed

45.

van Vulpen LFD, Popov-Celeketic J, van Meegeren MER, Coeleveld K, van Laar JM, Hack CE, Schutgens REG, Mastbergen SC, Lafeber FPJG (2017) A fusion protein of interleukin-4 and interleukin-10 protects against blood-induced cartilage damage in vitro and in vivo. J Thromb Haemost 15(9):1788–1798. https://doi.org/10.1111/jth.13778 CrossRefPubMed

46.

Waly NE, Refaiy A, Aborehab NM (2017) IL-10 and TGF-β: roles in chondroprotective effects of glucosamine in experimental osteoarthritis. Pathophysiology 24(1):45–49. https://doi.org/10.1016/j.pathophys.2017.02.005 CrossRefPubMed

47.

Martins DF, Turnes BL, Cidral-Filho FJ, Bobinski F, Rosas RF, Danielski LG, Petronilho F, Santos AR (2016) Light-emitting diode therapy reduces persistent inflammatory pain: role of interleukin 10 and antioxidant enzymes. Neuroscience 324:485–495. https://doi.org/10.1016/j.neuroscience.2016.03.035 CrossRefPubMed

48.

Helrigle C, de Carvalho PD, Casalechi HL, Leal-Junior EC, Fernandes GH, Helrigel PA, Rabelo RL, de Oliveira Aleixo-Junior I, Aimbire F, Albertini R (2016) Effects of low-intensity non-coherent light therapy on the inflammatory process in the calcaneal tendon of ovariectomized rats. Lasers Med Sci 31(1):33–40. https://doi.org/10.1007/s10103-015-1821-7 CrossRefPubMed

49.

Peat FJ, Colbath AC, Bentsen LM, Goodrich LR, King MR (2017) In vitro effects of high-intensity laser photobiomodulation on equine bone marrow-derived mesenchymal stem cell viability and cytokine expression. Photomed Laser Surg. https://doi.org/10.1089/pho.2017.4344

50.

Koh YG, Jo SB, Kwon OR, Suh DS, Lee SW, Park SH et al (2013) Mesenchymal stem cell injections improve symptoms of knee osteoarthritis. Arthroscopy 29:748–755. https://doi.org/10.1016/j.arthro.2012.11.017 CrossRefPubMed

51.

Frisbie DD, Kisiday JD, Kawcak CE, Werpy NM, McIlwraith CW (2009) Evaluation of adipose-derived stromal vascular fraction or bone marrow-derived mesenchymal stem cells for treatment of osteoarthritis. J Orthop Res 27(12):1675–1680. https://doi.org/10.1002/jor.20933 CrossRefPubMed

52.

Pallotta RC, Bjordal JM, Frigo L, Junior EC, Teixeira S, Marcos RL et al (2012) Infrared (810-nm) low-level laser therapy on rat experimental knee inflammation. Lasers Med Sci 27(1):71–78. https://doi.org/10.1007/s10103-011-0906-1 CrossRefPubMed

53.

Assis L, Milares LP, Almeida T, Tim C, Magri A, Fernandes KR et al (2016) Aerobic exercise training and low-level laser therapy modulate inflammatory response and degenerative process in an experimental model of knee osteoarthritis in rats. Osteoarthr Cartil 24(1):169–177. https://doi.org/10.1016/j.joca.2015.07.020 CrossRefPubMed

54.

Tomazoni SS, Leal-Junior EC, Pallotta RC, Teixeira S, de Almeida P, Lopes-Martins RÁ (2017) Effects of photobiomodulation therapy, pharmacological therapy, and physical exercise as single and/or combined treatment on the inflammatory response induced by experimental osteoarthritis. Lasers Med Sci 32(1):101–108. https://doi.org/10.1007/s10103-016-2091-8 CrossRefPubMed

55.

Sanches M, Assis L, Criniti C, Fernandes D, Tim C, Renno ACM (2017) Chondroitin sulfate and glucosamine sulfate associated to photobiomodulation prevents degenerative morphological changes in an experimental model of osteoarthritis in rats. Lasers Med Sci. https://doi.org/10.1007/s10103-017-2401-9

56.

Tomazoni SS, Leal-Junior EC, Frigo L, Pallotta RC, Teixeira S, de Almeida P, Bjordal JM, Lopes-Martins RÁ (2016) Isolated and combined effects of photobiomodulation therapy, topical nonsteroidal anti-inflammatory drugs, and physical activity in the treatment of osteoarthritis induced by papain. J Biomed Opt 21(10):108001. https://doi.org/10.1117/1.JBO.21.10.108001 CrossRefPubMed

57.

Park IS, Chung PS, Ahn JC (2015) Enhancement of ischemic wound healing by spheroid grafting of human adipose-derived stem cells treated with low-level light irradiation. PLoS One 10(6):e0122776. https://doi.org/10.1371/journal.pone.0122776 CrossRefPubMedPubMedCentral

58.

Spoto G, De Iuliis V, Petrini M, Flati V, Di Gregorio J, Vitale D et al (2016) Effect of low energy light irradiation by light emitting diode on U937 cells. J Biol Regul Homeost Agents 30(4):997–1007PubMed

59.

Barboza CAG, Ginani F, Soares DM, Henriques ÁCG, Freitas RA (2014) Low-level laser irradiation induces in vitro proliferation of mesenchymal stem cells. Einstein 12(1):75–81. https://doi.org/10.1590/S1679-45082014AO2824 CrossRefPubMedPubMedCentral

60.

Fekrazad R, Asefi S, Allahdadi M, Kalhori KA (2016) Effect of photobiomodulation on mesenchymal stem cells. Photomed Laser Surg 34(11):533–542CrossRefPubMed

Titel: Can photobiomodulation associated with implantation of mesenchymal adipose-derived stem cells attenuate the expression of MMPs and decrease degradation of type II collagen in an experimental model of osteoarthritis?
verfasst von: Tatiane Garcia Stancker
Stella Souza Vieira
Andrey Jorge Serra
Rafael do Nascimento Lima
Regiane dos Santos Feliciano
José Antônio Silva Jr.
Solange Almeida dos Santos
Marcia Ataize dos Santos Vieira
Maíra Cecília Brandão Simões
Ernesto Cesar Leal-Junior
Paulo de Tarso Camillo de Carvalho
Publikationsdatum: 08.03.2018
Verlag: Springer London
Erschienen in: Lasers in Medical Science / Ausgabe 5/2018
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-018-2466-0

Springer Medizin

Abstract

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