Cellular response to infrared radiation involves retrograde mitochondrial signaling.

Infrared A radiation (IRA) is a major component of sunlight. Similar to ultraviolet (UV) B and UVA, IRA induces gene transcription. In contrast to the UV response very little is known about the IRA response. In the present study, IRA-induced expression of matrix metalloproteinase-1 (MMP-1) was found to be mediated by the formation of intracellular reactive oxygen species (ROS). Staining of IRA-irradiated cells with MitoSox revealed an increase in mitochondrial superoxide anion production and treatment of fibroblasts with the mitochondrial targeted antioxidant MitoQ completely abrogated the IRA, but not the UVB or UVA1, response. ROS relevant for IRA-induced signaling originated from the mt electron transport chain, because (i) chemical inhibition of the electron transport chain prevented IRA, but not UVB or UVA1, radiation-induced MMP-1 expression, (ii) rho0 fibroblasts specifically failed to increase MMP-1 expression in response to IRA, and (iii) peroxisome proliferator-activated receptor gamma coactivator-1 (PGC-1) overexpressing fibroblasts with increased electron transport chain content were hypersensitive to IRA radiation-induced gene expression. Thus, IRA, in contrast to UV, elicits a retrograde signaling response in human skin.

[1]  J. Saffitz,et al.  Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. , 2000, The Journal of clinical investigation.

[2]  K. Wittern,et al.  In human keratinocytes the Common Deletion reflects donor variabilities rather than chronologic aging and can be induced by ultraviolet A irradiation. , 2001, The Journal of investigative dermatology.

[3]  T. Karu,et al.  Primary and secondary mechanisms of action of visible to near-IR radiation on cells. , 1999, Journal of photochemistry and photobiology. B, Biology.

[4]  T. Wirth,et al.  Overexpression of Phospholipid-hydroperoxide Glutathione Peroxidase in Human Dermal Fibroblasts Abrogates UVA Irradiation-induced Expression of Interstitial Collagenase/Matrix Metalloproteinase-1 by Suppression of Phosphatidylcholine Hydroperoxide-mediated NFκB Activation and Interleukin-6 Release* , 2004, Journal of Biological Chemistry.

[5]  Adnan Erol,et al.  Retrograde regulation due to mitochondrial dysfunction may be an important mechanism for carcinogenesis. , 2005, Medical hypotheses.

[6]  P. Schroeder,et al.  Premature Skin Aging by Infrared Radiation, Tobacco Smoke and Ozone , 2006 .

[7]  I. Kochevar,et al.  Ultraviolet A induces apoptosis via reactive oxygen species in a model for Smith-Lemli-Opitz syndrome. , 2006, Free radical biology & medicine.

[8]  T. Karu,et al.  A Novel Mitochondrial Signaling Pathway Activated by Visible-to-near Infrared Radiation¶ , 2004, Photochemistry and photobiology.

[9]  Michael N. Hall,et al.  TOR signalling in bugs, brain and brawn , 2003, Nature Reviews Molecular Cell Biology.

[10]  S. A. Gordon,et al.  Red and far-red action on oxidative phosphorylation. , 1960, Radiation research.

[11]  D. Sabatini,et al.  mTOR Interacts with Raptor to Form a Nutrient-Sensitive Complex that Signals to the Cell Growth Machinery , 2002, Cell.

[12]  Henrik Loevschall,et al.  Effect of low level diode laser irradiation of human oral mucosa fibroblasts in vitro , 1994, Lasers in surgery and medicine.

[13]  J. Joseph,et al.  Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. , 1999, Free radical biology & medicine.

[14]  Robin A. J. Smith,et al.  Selective Targeting of a Redox-active Ubiquinone to Mitochondria within Cells , 2001, The Journal of Biological Chemistry.

[15]  R. Tyrrell,et al.  Activation of mammalian gene expression by the UV component of sunlight – from models to reality , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[16]  Robin A. J. Smith,et al.  Mitochondria‐targeted antioxidants protect Friedreich Ataxia fibroblasts from endogenous oxidative stress more effectively than untargeted antioxidants , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[17]  G. Amuthan,et al.  Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells , 2002, Oncogene.

[18]  H. Esterbauer,et al.  Human peroxisome proliferator activated receptor gamma coactivator 1 (PPARGC1) gene: cDNA sequence, genomic organization, chromosomal localization, and tissue expression. , 1999, Genomics.

[19]  T. Karu,et al.  Cell attachment to extracellular matrices is modulated by pulsed radiation at 820 nm and chemicals that modify the activity of enzymes in the plasma membrane , 2001, Lasers in surgery and medicine.

[20]  Robin A. J. Smith,et al.  Prevention of Mitochondrial Oxidative Damage Using Targeted Antioxidants , 2002, Annals of the New York Academy of Sciences.

[21]  N. Avadhani,et al.  Mitochondrial signaling: the retrograde response. , 2004, Molecular cell.

[22]  B. Gilchrest,et al.  Photoaging of Skin , 2006 .

[23]  M. King,et al.  Isolation of human cell lines lacking mitochondrial DNA. , 1996, Methods in enzymology.

[24]  Philippa R. N. Wolohan,et al.  Highly Flexible Ligand Binding Pocket of Ecdysone Receptor , 2004, Journal of Biological Chemistry.

[25]  C. Harley,et al.  Extension of life-span by introduction of telomerase into normal human cells. , 1998, Science.

[26]  J. Johnson,et al.  Activation of transcription factor AP-2 mediates UVA radiation- and singlet oxygen-induced expression of the human intercellular adhesion molecule 1 gene. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Jean Krutmann,et al.  Cutaneous effects of infrared radiation: from clinical observations to molecular response mechanisms , 2003, Photodermatology, photoimmunology & photomedicine.

[28]  M. L. Genova,et al.  Role of Mitochondria in Oxidative Stress and Aging , 2002, Annals of the New York Academy of Sciences.

[29]  S. Grether-Beck,et al.  Infrared-A radiation-induced matrix metalloproteinase 1 expression is mediated through extracellular signal-regulated kinase 1/2 activation in human dermal fibroblasts. , 2002, The Journal of investigative dermatology.

[30]  J. Leeder,et al.  Use of a microplate reader in an assay of glutathione reductase using 5,5'-dithiobis(2-nitrobenzoic acid). , 1989, Analytical biochemistry.

[31]  M. King,et al.  Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. , 1989, Science.

[32]  T. Finkel,et al.  A role for mitochondria as potential regulators of cellular life span. , 2002, Biochemical and biophysical research communications.

[33]  T. Ruzicka,et al.  Singlet Oxygen Mediates the UVA-induced Generation of the Photoaging-associated Mitochondrial Common Deletion* , 1999, The Journal of Biological Chemistry.

[34]  J. Turrens Superoxide Production by the Mitochondrial Respiratory Chain , 1997, Bioscience reports.

[35]  J. Murat,et al.  Implication of free radicals and glutathione in the mechanism of cadmium-induced expression of stress proteins in the A549 human lung cell-line. , 2000, Biochimica et biophysica acta.

[36]  S. Grether-Beck,et al.  Ultraviolet A radiation-induced expression of human genes: molecular and photobiological mechanisms. , 1997, Biological chemistry.

[37]  P. Sacchetta,et al.  Alkaline hydrolysis of N-ethylmaleimide allows a rapid assay of glutathione disulfide in biological samples. , 1986, Analytical biochemistry.

[38]  S. Grether-Beck,et al.  Mitochondrial Cytochrome c Release Mediates Ceramide-induced Activator Protein 2 Activation and Gene Expression in Keratinocytes* , 2003, Journal of Biological Chemistry.

[39]  T. Karu,et al.  Cell attachment modulation by radiation from a pulsed light diode (λ = 820 nm) and various chemicals , 2001 .

[40]  L. Declercq,et al.  Creatine supplementation normalizes mutagenesis of mitochondrial DNA as well as functional consequences. , 2005, The Journal of investigative dermatology.

[41]  C. Elger,et al.  Characterization of Superoxide-producing Sites in Isolated Brain Mitochondria* , 2004, Journal of Biological Chemistry.

[42]  P. Herrlich,et al.  UV-induced signal transduction. , 1997, Journal of photochemistry and photobiology. B, Biology.

[43]  K. Scharffetter-Kochanek,et al.  Ultraviolet‐B Irradiation and Matrix Metalloproteinases , 2002 .

[44]  K. Wolff,et al.  Fitzpatrick's Dermatology in General Medicine. 7th Edition , 2008 .

[45]  H. Shimizu,et al.  Ultraviolet A-induced Production of Matrix Metalloproteinase-1 Is Mediated by Macrophage Migration Inhibitory Factor (MIF) in Human Dermal Fibroblasts* , 2004, Journal of Biological Chemistry.

[46]  B. Freedman,et al.  Retrograde Ca2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter‐organelle crosstalk , 1999, The EMBO journal.