Korean J Physiol Pharmacol.  2019 Mar;23(2):141-150. 10.4196/kjpp.2019.23.2.141.

Far-infrared radiation stimulates platelet-derived growth factor mediated skeletal muscle cell migration through extracellular matrix-integrin signaling

Affiliations
  • 1Department of Physiology, Chung-Ang University College of Medicine, Seoul 06974, Korea. akdongyi01@cau.ac.kr
  • 2Department of Family Medicine, Chung-Ang University Hospital, Chung-Ang University College of Medicine, Seoul 06973, Korea. girlpower219@cau.ac.kr

Abstract

Despite increased evidence of bio-activity following far-infrared (FIR) radiation, susceptibility of cell signaling to FIR radiation-induced homeostasis is poorly understood. To observe the effects of FIR radiation, FIR-radiated materials-coated fabric was put on experimental rats or applied to L6 cells, and microarray analysis, quantitative real-time polymerase chain reaction, and wound healing assays were performed. Microarray analysis revealed that messenger RNA expressions of rat muscle were stimulated by FIR radiation in a dose-dependent manner in amount of 10% and 30% materials-coated. In 30% group, 1,473 differentially expressed genes were identified (fold change [FC] > 1.5), and 218 genes were significantly regulated (FC > 1.5 and p < 0.05). Microarray analysis showed that extracellular matrix (ECM)-receptor interaction, focal adhesion, and cell migration-related pathways were significantly stimulated in rat muscle. ECM and platelet-derived growth factor (PDGF)-mediated cell migration-related genes were increased. And, results showed that the relative gene expression of actin beta was increased. FIR radiation also stimulated actin subunit and actin-related genes. We observed that wound healing was certainly promoted by FIR radiation over 48 h in L6 cells. Therefore, we suggest that FIR radiation can penetrate the body and stimulate PDGF-mediated cell migration through ECM-integrin signaling in rats.

Keyword

Cell movement; Infrared rays; Integrins; Microarray analysis; Platelet-derived growth factor

MeSH Terms

Actins
Animals
Cell Movement*
Extracellular Matrix
Focal Adhesions
Gene Expression
Homeostasis
Infrared Rays
Integrins
Microarray Analysis
Muscle, Skeletal*
Platelet-Derived Growth Factor*
Rats
Real-Time Polymerase Chain Reaction
RNA, Messenger
Wound Healing
Actins
Integrins
Platelet-Derived Growth Factor
RNA, Messenger

Figure

  • Fig. 1 Microarray analysis of messenger RNA expression in bio-active materials-coated fabric and control rat. (A) Hierarchical clustering heatmap was classified as color based on differentially expressed genes between Test10 group (10% materials-coated fabric), Test30 groups (30% materials-coated fabric) and control group. Yellow and blue color represents higher and lower than z-score mean. (B) Up- and down-regulated genes count were indicated each group (fold change [FC] > 1.5 and 2). (C) Significant genes count was indicated each group (FC < 1.5 and < 2, p < 0.05).

  • Fig. 2 Protein interaction network analysis. Protein interaction network was identified upon 22 differentially expressed genes via Search Tool for the Retrieval of Interacting Genes version 10.5 (STRING; www.string-db.org). Col6a1, collagen, type VI alpha 1; Col3a1, collagen, type 3, alpha 1; Nid1, nidogen 1; Bgn, biglycan; Mmp14, matrix metallopeptidase 14; Actb, actin beta; Mmp2, matrix metallopeptidase 2; Vim, vimentin; Cd34, cd34 molecule; Msn, moesin; Gsn, gelsolin; Lcp1, lymphocyte cytosolic protein 1; Bmp4, bone morphogenetic protein 4; Sparc, secreted protein acidic cysteinerich; Pdgfra, platelet-derived growth factor receptor alpha polypeptide; Igf1, insulin-like growth factor 1; Tgfb1, transforming growth factor beta 1; Plau, plasminogen activator urokinase; Lrp1, low density lipoprotein receptor-related protein 1; Csf1r, colony stimulating factor 1 receptor; Rarres2, retinoic acid receptor responder 2; Apoe, apolipoprotein E.

  • Fig. 3 Expression of messenger RNA for platelet-derived growth factor (PDGF)-mediated cell migration-related genes. (A) PDGF D (Pdgfd), (B) PDGF receptor alpha (Pdgfra), (C) PDGF receptor-like (Pdgfrl), (D) extracellular matrix protein 1 (Ecm1), (E) extracellular matrix protein 2 (Ecm2), (F) matrix metallopeptidase 2 (Mmp2), (G) integrin alpha 5 (Itga5), and (H) actin beta (Actb). FIR, far-infrared. *Statistically significant vs. control group, p < 0.05; **statistically significant vs. control group, p < 0.01.

  • Fig. 4 Wound healing assay using L6 cells of 0% and 10% far-infrared (FIR) radiated fabric for 48 h. (A) Images of L6 cell for 0% and 10% FIR radiated fabric were captured upon 0, 24, and 48 h in wound healing assay. (B) Relative scratch gap area was based on 0 h in 0% materials-coated fabric group cell and which were calculated using Image J software. **Statistically significant vs. control group, p < 0.01.


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Reference

1. Yu SY, Chiu JH, Yang SD, Hsu YC, Lui WY, Wu CW. Biological effect of far-infrared therapy on increasing skin microcirculation in rats. Photodermatol Photoimmunol Photomed. 2006; 22:78–86.
Article
2. Beever R. Far-infrared saunas for treatment of cardiovascular risk factors: summary of published evidence. Can Fam Physician. 2009; 55:691–696.
3. Adamskaya N, Dungel P, Mittermayr R, Hartinger J, Feichtinger G, Wassermann K, Redl H, van Griensven M. Light therapy by blue LED improves wound healing in an excision model in rats. Injury. 2011; 42:917–921.
Article
4. Vatansever F, Hamblin MR. Far infrared radiation (FIR): its biological effects and medical applications. Photonics Lasers Med. 2012; 4:255–266.
Article
5. Tsai SR, Hamblin MR. Biological effects and medical applications of infrared radiation. J Photochem Photobiol B. 2017; 170:197–207.
Article
6. Inoué S, Kabaya M. Biological activities caused by far-infrared radiation. Int J Biometeorol. 1989; 33:145–150.
Article
7. Rau CS, Yang JC, Jeng SF, Chen YC, Lin CJ, Wu CJ, Lu TH, Hsieh CH. Far-infrared radiation promotes angiogenesis in human microvascular endothelial cells via extracellular signal-regulated kinase activation. Photochem Photobiol. 2011; 87:441–446.
Article
8. Tran TH, Mai HN, Shin EJ, Nam Y, Nguyen BT, Lee YJ, Jeong JH, Tran HY, Cho EH, Nah SY, Lei XG, Nabeshima T, Kim NH, Kim HC. Repeated exposure to far infrared ray attenuates acute restraint stress in mice via inhibition of JAK2/STAT3 signaling pathway by induction of glutathione peroxidase-1. Neurochem Int. 2016; 94:9–22.
Article
9. Huang PH, Chen JW, Lin CP, Chen YH, Wang CH, Leu HB, Lin SJ. Far infra-red therapy promotes ischemia-induced angiogenesis in diabetic mice and restores high glucose-suppressed endothelial progenitor cell functions. Cardiovasc Diabetol. 2012; 11:99.
Article
10. Yang CS, Yeh CH, Tung CL, Chen MY, Jiang CH, Yeh ML. Impact of far-infrared ray exposure on the mechanical properties of unwounded skin of rats. Exp Biol Med (Maywood). 2010; 235:952–956.
Article
11. Shui S, Wang X, Chiang JY, Zheng L. Far-infrared therapy for cardiovascular, autoimmune, and other chronic health problems: a systematic review. Exp Biol Med (Maywood). 2015; 240:1257–1265.
12. Hsu YH, Chen YC, Chen TH, Sue YM, Cheng TH, Chen JR, Chen CH. Far-infrared therapy induces the nuclear translocation of PLZF which inhibits VEGF-induced proliferation in human umbilical vein endothelial cells. PLoS One. 2012; 7:e30674.
Article
13. Noponen PVA, Häkkinen K, Mero AA. Effects of far infrared heat on recovery in power athletes. J Athl Enhancement. 2015; 4:DOI: 10.4172/2324-9080.1000202.
Article
14. Mai HN, Sharma N, Shin EJ, Nguyen BT, Nguyen PT, Jeong JH, Jang CG, Cho EH, Nah SY, Kim NH, Nabeshima T, Kim HC. Exposure to far-infrared rays attenuates methamphetamine-induced recognition memory impairment via modulation of the muscarinic M1 receptor, Nrf2, and PKC. Neurochem Int. 2018; 116:63–76.
Article
15. Chang HY, Shih MH, Huang HC, Tsai SR, Juan HF, Lee SC. Middle infrared radiation induces G2/M cell cycle arrest in A549 lung cancer cells. PLoS One. 2013; 8:e54117.
Article
16. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. Cell migration: integrating signals from front to back. Science. 2003; 302:1704–1709.
Article
17. Sheetz MP, Felsenfeld DP, Galbraith CG. Cell migration: regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol. 1998; 8:51–54.
Article
18. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer. 2002; 2:91–100.
Article
19. Krawczyk C, Oliveira-dos-Santos A, Sasaki T, Griffiths E, Ohashi PS, Snapper S, Alt F, Penninger JM. Vav1 controls integrin clustering and MHC/peptide-specific cell adhesion to antigen-presenting cells. Immunity. 2002; 16:331–343.
Article
20. Blazevic T, Schwaiberger AV, Schreiner CE, Schachner D, Schaible AM, Grojer CS, Atanasov AG, Werz O, Dirsch VM, Heiss EH. 12/15-lipoxygenase contributes to platelet-derived growth factor-induced activation of signal transducer and activator of transcription 3. J Biol Chem. 2013; 288:35592–35603.
21. Alvarez RH, Kantarjian HM, Cortes JE. Biology of platelet-derived growth factor and its involvement in disease. Mayo Clin Proc. 2006; 81:1241–1257.
Article
22. Yu J, Moon A, Kim HR. Both platelet-derived growth factor receptor (PDGFR)-alpha and PDGFR-beta promote murine fibroblast cell migration. Biochem Biophys Res Commun. 2001; 282:697–700.
23. Robbins JR, McGuire PG, Wehrle-Haller B, Rogers SL. Diminished matrix metalloproteinase 2 (MMP-2) in ectomesenchyme-derived tissues of the Patch mutant mouse: regulation of MMP-2 by PDGF and effects on mesenchymal cell migration. Dev Biol. 1999; 212:255–263.
Article
24. Xu J, Clark RA. Extracellular matrix alters PDGF regulation of fibroblast integrins. J Cell Biol. 1996; 132:239–249.
Article
25. Zhang F, Hao F, An D, Zeng L, Wang Y, Xu X, Cui MZ. The matricellular protein Cyr61 is a key mediator of platelet-derived growth factor-induced cell migration. J Biol Chem. 2015; 290:8232–8242.
Article
26. Li J, Kim YN, Bertics PJ. Platelet-derived growth factor-stimulated migration of murine fibroblasts is associated with epidermal growth factor receptor expression and tyrosine phosphorylation. J Biol Chem. 2000; 275:2951–2958.
Article
27. Raines EW, Lane TF, Iruela-Arispe ML, Ross R, Sage EH. The extracellular glycoprotein SPARC interacts with platelet-derived growth factor (PDGF)-AB and -BB and inhibits the binding of PDGF to its receptors. Proc Natl Acad Sci U S A. 1992; 89:1281–1285.
Article
28. Yuan L, Santi M, Rushing EJ, Cornelison R, MacDonald TJ. ERK activation of p21 activated kinase-1 (Pak1) is critical for medulloblastoma cell migration. Clin Exp Metastasis. 2010; 27:481–491.
Article
29. MacDonald TJ, Brown KM, LaFleur B, Peterson K, Lawlor C, Chen Y, Packer RJ, Cogen P, Stephan DA. Expression profiling of medulloblastoma: PDGFRA and the RAS/MAPK pathway as therapeutic targets for metastatic disease. Nat Genet. 2001; 29:143–152.
Article
30. Borkham-Kamphorst E, van Roeyen CR, Ostendorf T, Floege J, Gressner AM, Weiskirchen R. Pro-fibrogenic potential of PDGF-D in liver fibrosis. J Hepatol. 2007; 46:1064–1074.
Article
31. Veevers-Lowe J, Ball SG, Shuttleworth A, Kielty CM. Mesenchymal stem cell migration is regulated by fibronectin through α5β1-integrin-mediated activation of PDGFR-β and potentiation of growth factor signals. J Cell Sci. 2011; 124:1288–1300.
Article
32. Schlaepfer DD, Hanks SK, Hunter T, van der Geer P. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature. 1994; 372:786–791.
Article
33. Cingolani LA, Goda Y. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci. 2008; 9:344–356.
Article
34. Vicente-Manzanares M, Choi CK, Horwitz AR. Integrins in cell migration--the actin connection. J Cell Sci. 2009; 122:199–206.
35. Peterson EJ. The TCR ADAPts to integrin-mediated cell adhesion. Immunol Rev. 2003; 192:113–121.
Article
36. Hsu YH, Lin YF, Chen CH, Chiu YJ, Chiu HW. Far infrared promotes wound healing through activation of Notch1 signaling. J Mol Med (Berl). 2017; 95:1203–1213.
Article
37. Lee D, Kim YW, Kim JH, Yang M, Bae H, Lim I, Bang H, Go KC, Yang GW, Rho YH, Park HS, Park EH, Ko JH. Improvement characteristics of bio-active materials coated fabric on rat muscular mitochondria. Korean J Physiol Pharmacol. 2015; 19:283–289.
Article
38. Lee SG, Lee CG, Wu HM, Oh CS, Chung SW, Kim SG. A load of mice to hypergravity causes AMPKα repression with liver injury, which is overcome by preconditioning loads via Nrf2. Sci Rep. 2015; 5:15643.
Article
39. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015; 43:D447–D452.
Article
40. Henderson TA, Morries LD. Near-infrared photonic energy penetration: can infrared phototherapy effectively reach the human brain? Neuropsychiatr Dis Treat. 2015; 11:2191–2208.
Article
41. Zhu J, Clark RAF. Fibronectin at select sites binds multiple growth factors and enhances their activity: expansion of the collaborative ECM-GF paradigm. J Invest Dermatol. 2014; 134:895–901.
Article
42. Laurent M, Martinerie C, Thibout H, Hoffman MP, Verrecchia F, Le Bouc Y, Mauviel A, Kleinman HK. NOVH increases MMP3 expression and cell migration in glioblastoma cells via a PDGFR-alphadependent mechanism. FASEB J. 2003; 17:1919–1921.
43. Hardee JP, Puppa MJ, Fix DK, Gao S, Hetzler KL, Bateman TA, Carson JA. The effect of radiation dose on mouse skeletal muscle remodeling. Radiol Oncol. 2014; 48:247–256.
Article
44. Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR. The laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alpha3 isoform. J Cell Biol. 1997; 137:685–701.
45. Boraschi-Diaz I, Wang J, Mort JS, Komarova SV. Collagen type I as a ligand for receptor-mediated signaling. Front Phys. 2017; 5:DOI: 10.3389/fphy.2017.00012.
Article
46. Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 1992; 70:389–399.
Article
47. Duchek P, Somogyi K, Jékely G, Beccari S, Rørth P. Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell. 2001; 107:17–26.
Article
48. Le Clainche C, Carlier MF. Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev. 2008; 88:489–513.
Article
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