Top

Published in:

26-09-2022 | Arthritis | Original Article

Photobiomodulation effects in metalloproteinases expression in zymosan-induced arthritis

Authors: Lucia Mara Januário dos Anjos, Anna Cecília Quirino-Teixeira, Eugenio Damasceno Hottz, Adenilson de Souza da Fonseca, Jacy Gameiro, Flávia de Paoli

Published in: Lasers in Medical Science | Issue 9/2022

Abstract

Matrix metalloproteinases (MMPs) play a crucial role in the degenerative course of rheumatic disorders. They are responsible for cartilage and other joint-associated tissues breakdown. Amid arthritis treatments, photobiostimulation (PBM), a non-thermal and non-invasive low-power laser application, appears to be an outstanding therapy alternative once it has succeeded in MMPs modulation. Thus, this study aimed to evaluate the PBM effects of low infrared laser (830 nm), testing two different energy densities (3 and 30 Jcm⁻²) in MMP-2, MMP-9, MMP-13, and MMP-14 as well as the inhibitor TIMP-2 expressions using zymosan-induced arthritis model. C57BL/6 mice were distributed into four groups (n = 8): zymosan-induced arthritis without treatment; zymosan-induced arthritis and dexamethasone-treated; zymosan-induced arthritis and PBM at energy density of 3 Jcm⁻² treated; and zymosan-induced arthritis and PBM at energy density of 30 Jcm⁻² treated. MMPs and TIMP-2 mRNA relative levels by qRT-PCR and proteins expression by immunohistochemical and Western blotting techniques were performed after PBM treatment in the inflamed joint. Our results demonstrated PBM could modulate both mRNA relative levels and proteins expression of the MMP-2, -9, -13, -14, and TIMP-2 in joint tissues, decreasing MMP-9 protein expression and increasing TIMP-2 protein expression. PBM promotes a better arthritis prognostic, modulating metalloproteinase and its inhibitor, especially MMP-9 and TIMP-2 protein expression that is important inflammatory markers. These findings may also corroborate that PBM may regulate MMPs expression using different pathways.

Orr C, Sousa E, Boyle DL et al (2017) Synovial tissue research: a state-of-the-art review. Nat Rev Rheumatol 13(8):463–475. https://doi.org/10.1038/nrrheum.2017.115CrossRefPubMed

Scanzello CR, Goldring SR (2012) The role of synovitis in osteoarthritis pathogenesis. Bone 51(2):249–257. https://doi.org/10.1016/j.bone.2012.02.012CrossRefPubMedPubMedCentral

Firestein GS, McInnes IB (2017) Immunopathogenesis of rheumatoid arthritis. Immunity 46(2):183–196. https://doi.org/10.1016/j.immuni.2017.02.006CrossRefPubMedPubMedCentral

Croft AP, Campos J, Jansen K et al (2019) Distinct fibroblast subsets drive inflammation and damage in arthritis. Nature 570(7760):246–251. https://doi.org/10.1038/s41586-019-1263-7CrossRefPubMedPubMedCentral

Udalova IA, Mantovani A, Feldmann M (2016) Macrophage heterogeneity in the context of rheumatoid arthritis. Nat Rev Rheumatol 12(8):472–485. https://doi.org/10.1038/nrrheum.2016.91CrossRefPubMed

McInnes SG (2007) Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol 7(6):429–442. https://doi.org/10.1038/nri2094CrossRefPubMed

Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233. https://doi.org/10.1038/nrm2125CrossRefPubMedPubMedCentral

Vandenbroucke RE, Libert C (2014) Is there new hope for therapeutic matrix metalloproteinase inhibition? Nat Rev Drug Discov 13(12):904–927. https://doi.org/10.1038/nrd4390CrossRefPubMed

Murphy G, Knäuper V, Atkinson S et al (2002) Matrix metalloproteinases in arthritic disease. Arthritis Res 4:S39–S49. https://doi.org/10.1038/nrd4390CrossRefPubMedPubMedCentral

10.

Yoshihara Y, Nakamura H, Obata K et al (2000) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids from patients with rheumatoid arthritis or osteoarthritis. Ann Rheum Dis 59(6):455–461. https://doi.org/10.1136/ard.59.6.455CrossRefPubMedPubMedCentral

11.

Murphy G, Nagase H (2008) Reappraising metalloproteinases in rheumatoid arthritis and osteoarthritis: destruction or repair? Nat Clin Pract Rheumatol 4(3):128–135. https://doi.org/10.1038/ncprheum0727CrossRefPubMed

12.

Scott DL, Wolfe F, Huizinga TWJ (2010) Rheumatoid arthritis. Lancet 376(9746):1094–1108. https://doi.org/10.1016/S0140-6736(10)60826-4CrossRefPubMed

13.

Karu T (2010) Mitochondrial mechanisms of photobiomodulation in context of new data about multiple roles of ATP. Photomed Laser Surg 28(2):159–160. https://doi.org/10.1089/pho.2010.2789CrossRefPubMed

14.

Gao X, Xing D (2009) Molecular mechanisms of cell proliferation induced by low power laser irradiation. J Biomed Sci 16(1):31–37. https://doi.org/10.1186/1423-0127-16-4CrossRef

15.

dos Anjos LMJ, da Fonseca A, de S, Gameiro J, de Paoli F, (2017) Apoptosis induced by low-level laser in polymorphonuclear cells of acute joint inflammation: comparative analysis of two energy densities. Lasers Med Sci 32(5):975–983. https://doi.org/10.1007/s10103-017-2196-8CrossRefPubMed

16.

Alves ACA, Albertini R, Dos Santos SA 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-xCrossRefPubMed

17.

Chen C-H, Tsai J-L, Wang Y-H, Lee C-L, Chen J-K, Huang M-H (2009) Low-level laser irradiation promotes cell proliferation and mRNA expression of type I collagen and decorin in porcine achilles tendon fibroblasts in vitro. J Orthop Res 27(5):646–650. https://doi.org/10.1002/jor.20800CrossRefPubMed

18.

Pallotta RC, Bjordal JM, Frigo L 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/s10103-011-0906-1CrossRefPubMed

19.

Poppi RR, Da Silva AL, Nacer RS et al (2011) Evaluation of the osteogenic effect of low-level laser therapy (808 nm and 660 nm) on bone defects induced in the femurs of female rats submitted to ovariectomy. Lasers Med Sci 26(4):515–522. https://doi.org/10.1007/s10103-010-0867-9CrossRef

20.

Samoilova KA, Zhevago NA, Petrishchev NN, Zimin AA (2008) Role of nitric oxide in the visible light-induced rapid increase of human skin microcirculation at the local and systemic levels: II. Healthy volunteers Photomed Laser Surg 26(5):443–449. https://doi.org/10.1089/pho.2007.2205CrossRefPubMed

21.

Song JW, Li K, Liang ZW et al (2017) Low-level laser facilitates alternatively activated macrophage/microglia polarization and promotes functional recovery after crush spinal cord injury in rats. Sci Rep 7(1):1–13. https://doi.org/10.1038/s41598-017-00553-6CrossRef

22.

Abduch TF, da Silva PAV, de Souza AC, dos Anjos LMJ, et al. (2020) Evaluation of metalloproteinases-2, -9, and -13 post photobiomodulation in mice talocrural joint. 35(3): 633–640. https://doi.org/10.1007/s10103-019-02860-y

23.

dos Anjos LMJ, Salvador PA, de Souza ÁC et al (2019) Modulation of immune response to induced-arthritis by low-level laser therapy. J Biophotonics 12(2):1–12. https://doi.org/10.1002/jbio.201800120CrossRef

24.

Guerra FDR, Vieira CP, Almeida MS et al (2013) LLLT improves tendon healing through increase of MMP activity and collagen synthesis. Lasers Med Sci 28(5):1281–1288. https://doi.org/10.1007/s10103-012-1236-7CrossRefPubMed

25.

Huang Y-Y, Sharma SK, Carroll J, Hamblin MR (2011) Biphasic dose response in low level light therapy — an update. Dose-Response 9(4):602–618. https://doi.org/10.2203/dose-response.11-009.HamblinCrossRefPubMedPubMedCentral

26.

da Silva PAV, Dos Anjos LMJ, Abduch TF, Pereira R, da Fonsecade S, de Paoli F, A (2019) Photobiomodulation can alter mRNA levels cell death-related. Lasers Med Sci 34(7):1373–1380. https://doi.org/10.1007/s10103-019-02732-5CrossRefPubMed

27.

Dimitrova P, Ivanovska N, Schwaeble W, Gyurkovska V, Stover C (2010) The role of properdin in murine zymosan-induced arthritis. Mol Immunol 47(7–8):1458–1466. https://doi.org/10.1016/j.molimm.2010.02.007CrossRefPubMed

28.

Castano AP, Dai T, Yaroslavsky I et al (2007) Low-level laser therapy for zymosan-induced arthritis in rats: importance of illumination time. Lasers Med Sci 39(6):543–550. https://doi.org/10.1002/lsm.20516CrossRef

29.

Untergasser A, Cutcutache I, Koressaar T et al (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40(15):1–12. https://doi.org/10.1093/nar/gks596CrossRef

30.

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262CrossRefPubMed

31.

Gegout P, Gillet P, Chevrier D, Guingamp C, Terlain B, Netter P (1994) Characterization of zymosan-induced arthritis in the rat: effects on joint inflammation and cartilage metabolism. Life Sci 55(17):321–326. https://doi.org/10.1016/0024-3205(94)00771-3CrossRef

32.

Frasnelli ME, Tarussio D, Chobaz-Péclat V, Busso N, So A (2005) TLR2 modulates inflammation in zymosan-induced arthritis in mice. Arthritis Res Ther 7(2):R370–R379. https://doi.org/10.1186/ar1494CrossRefPubMedPubMedCentral

33.

Karu T (1999) Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B Biol 49(1):1–17. https://doi.org/10.1016/S1011-1344(98)00219-XCrossRef

34.

Burrage PS, Mix KS, Brinckerhoff CE (2006) Matrix metalloproteinases: role in arthritis. Front Biosci 11(1):529. https://doi.org/10.2741/1817CrossRefPubMed

35.

McInnes IB, Schett G (2017) Pathogenetic insights from the treatment of rheumatoid arthritis. Lancet 389(10086):2328–2337. https://doi.org/10.1016/S0140-6736(17)31472-1CrossRefPubMed

36.

Sabeh F, Fox D, Weiss SJ (2010) Membrane-type I matrix metalloproteinase-dependent regulation of rheumatoid arthritis synoviocyte function. J Immunol 184(11):6396–6406. https://doi.org/10.4049/jimmunol.0904068CrossRefPubMed

37.

Rose BJ, Kooyman DL (2016) A tale of two joints: the role of matrix metalloproteases in cartilage biology. Dis Markers 2016:4895050. https://doi.org/10.1155/2016/4895050CrossRefPubMedPubMedCentral

38.

Asif Amin M, Fox DA, Ruth JH (2017) Synovial cellular and molecular markers in rheumatoid arthritis. Semin Immunopathol 39(4):385–393. https://doi.org/10.1007/s00281-017-0631-3CrossRefPubMedPubMedCentral

39.

Fanjul-Fernández M, Folgueras AR, Cabrera S (1803) López-Otín C (2010) Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models. Biochim Biophys Acta - Mol Cell Res 1:3–19. https://doi.org/10.1016/j.bbamcr.2009.07.004CrossRef

40.

Ram M, Sherer Y, Shoenfeld Y (2006) Matrix metalloproteinase-9 and autoimmune diseases. J Clin Immunol 26(4):299–307. https://doi.org/10.1007/s10875-006-9022-6CrossRefPubMed

41.

Ruhul Amin ARM, Senga T, Oo ML, Thant AA, Hamaguchi M (2003) Secretion of matrix metalloproteinase-9 by the proinflammatory cytokine, IL-1β: a role for the dual signalling pathways. Akt and Erk Genes Cells 8(6):515–523. https://doi.org/10.1046/j.1365-2443.2003.00652.xCrossRefPubMed

42.

Zhou L, Yan C, Gieling RG et al (2009) Tumor necrosis factor-alpha induced expression of matrix metalloproteinase-9 through p21-activated kinase-1. BMC Immunol 19:10–15. https://doi.org/10.1186/1471-2172-10-15CrossRef

43.

Ray A, Bal BS, Ray BK (2005) Transcriptional induction of matrix metalloproteinase-9 in the chondrocyte and synoviocyte cells is regulated via a novel mechanism: evidence for functional cooperation between serum amyloid A—activating factor-1 and AP-1. J Immunol 175(6):4039–4048. https://doi.org/10.4049/jimmunol.175.6.4039CrossRefPubMed

44.

Yamanaka H, Makino K, Takizawa M et al (2000) Expression and tissue localization of metalloproteinases in rheumatoid Synovium 80(5):677–687. https://doi.org/10.1038/labinvest.3780071CrossRef

Title: Photobiomodulation effects in metalloproteinases expression in zymosan-induced arthritis
Authors: Lucia Mara Januário dos Anjos
Anna Cecília Quirino-Teixeira
Eugenio Damasceno Hottz
Adenilson de Souza da Fonseca
Jacy Gameiro
Flávia de Paoli
Publication date: 26-09-2022
Publisher: Springer London
Keywords: Arthritis
Dexamethasone
Laser
Published in: Lasers in Medical Science / Issue 9/2022
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-022-03647-4

At a glance: The STEP trials

Springer Medicine

Photobiomodulation effects in metalloproteinases expression in zymosan-induced arthritis

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 9/2022

Core outcome sets in clinical laser research: how better evidence can be better for patients

Effectiveness of electrophysical agents for treating pressure injuries: a systematic review

Effects of different protocols of defocused high-power laser on the viability and migration of myoblasts—a comparative in vitro study

Micro-Raman spectroscopy study of blood samples from myocardial infarction patients

The combined use of photobiomodulation and curcumin-loaded iron oxide nanoparticles significantly improved wound healing in diabetic rats compared to either treatment alone

The effects of photobiomodulation therapy in individuals with tinnitus and without hearing loss