New Insights into the Implication of Mitochondrial Dysfunction in Tissue, Peripheral Blood Mononuclear Cells, and Platelets during Lung Diseases
Abstract
1. Introduction
2. Physiological Mitochondrial Function
3. Mitochondrial Dysfunction in Lung Diseases
3.1. Chronic Obstructive Pulmonary Disease (COPD)
3.1.1. Mitochondrial Dysfunction and Oxidative Stress in COPD
3.1.2. Mitochondrial Function, Oxidative Stress, and mtDNA in PBMCs or Platelets in COPD
3.2. Asthma
3.2.1. Mitochondrial Function and Oxidative Stress in Asthma
3.2.2. Enhanced Mitochondrial Function and ROS Production in PBMCs or Platelets in Asthma
3.3. Pulmonary Hypertension
3.3.1. Mitochondrial Dysfunction, ROS, and mtDNA in Pulmonary Hypertension
3.3.2. Mitochondrial Function in Platelets during Pulmonary Hypertension
3.4. Idiopathic Pulmonary Fibrosis and Interstitial Lung Diseases
Mitochondrial Dysfunction, Oxidative Stress, and Inflammation in Idiopathic Pulmonary Fibrosis
4. Connections between Mitochondrial Dysfunction, ROS, and Inflammatory/Fibrotic Pathways in Lung Diseases. Pathophysiological Hypothesis
5. Antioxidative Therapies
6. Conclusions
Funding
Acknowledgments
Conflicts of Interest
References
- Lopez-Campos, J.L.; Tan, W.; Soriano, J.B. Global burden of COPD. Respirology 2016, 21, 14–23. [Google Scholar] [CrossRef] [PubMed]
- Loftus, P.A.; Wise, S.K. Epidemiology and economic burden of asthma. Int. Forum Allergy Rhinol. 2015, 5, S7–S10. [Google Scholar] [CrossRef] [PubMed]
- Tran, T.; Sterclova, M.; Mogulkoc, N.; Lewandowska, K.; Muller, V.; Hajkova, M.; Kramer, M.R.; Jovanovic, D.; Tekavec-Trkanjec, J.; Studnicka, M.; et al. The European MultiPartner IPF registry (EMPIRE): Validating long-term prognostic factors in idiopathic pulmonary fibrosis. Respir. Res. 2020, 21, 11. [Google Scholar] [CrossRef] [PubMed]
- Hurdman, J.; Condliffe, R.; Elliot, C.A.; Davies, C.; Hill, C.; Wild, J.M.; Capener, D.; Sephton, P.; Hamilton, N.; Armstrong, I.J.; et al. ASPIRE registry: Assessing the spectrum of pulmonary hypertension identified at a REferral centre. Eur. Respir. J. 2012, 39, 945–955. [Google Scholar] [CrossRef] [PubMed]
- Alfatni, A.; Riou, M.; Charles, A.-L.; Meyer, A.; Barnig, C.; Andres, E.; Lejay, A.; Talha, S.; Geny, B. Peripheral blood mononuclear cells and platelets mitochondrial dysfunction, oxidative stress, and circulating mtdna in cardiovascular diseases. J. Clin. Med. 2020, 9. [Google Scholar] [CrossRef] [PubMed]
- Coluccia, R.; Raffa, S.; Ranieri, D.; Micaloni, A.; Valente, S.; Salerno, G.; Scrofani, C.; Testa, M.; Gallo, G.; Pagannone, E.; et al. Chronic heart failure is characterized by altered mitochondrial function and structure in circulating leucocytes. Oncotarget 2018, 9, 35028–35040. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Li, P.; Wang, B.; Sun, F.; Li, Y.; Li, Q.; Lang, H.; Zhao, Z.; Gao, P.; Zhao, Y.; Shang, Q.; et al. Mitochondrial respiratory dysfunctions of blood mononuclear cells link with cardiac disturbance in patients with early-stage heart failure. Sci. Rep. 2015, 5, 10229. [Google Scholar] [CrossRef]
- Ijsselmuiden, A.J.J.; Musters, R.J.P.; de Ruiter, G.; van Heerebeek, L.; Alderse-Baas, F.; van Schilfgaarde, M.; Leyte, A.; Tangelder, G.-J.; Laarman, G.J.; Paulus, W.J.; et al. Circulating white blood cells and platelets amplify oxidative stress in heart failure. Nat. Clin. Pract. Cardiovasc. Med. 2008, 5, 811–820. [Google Scholar] [CrossRef]
- Adrie, C.; Bachelet, M.; Vayssier-Taussat, M.; Russo-Marie, F.; Bouchaert, I.; Adib-Conquy, M.; Cavaillon, J.M.; Pinsky, M.R.; Dhainaut, J.F.; Polla, B.S.; et al. Mitochondrial membrane potential and apoptosis peripheral blood monocytes in severe human sepsis. Am. J. Respir. Crit. Care Med. 2001, 164, 389–395. [Google Scholar] [CrossRef]
- Belikova, I.; Lukaszewicz, A.C.; Faivre, V.; Damoisel, C.; Singer, M.; Payen, D. Oxygen consumption of human peripheral blood mononuclear cells in severe human sepsis. Crit. Care Med. 2007, 35, 2702–2708. [Google Scholar] [CrossRef]
- Garrabou, G.; Moren, C.; Lopez, S.; Tobias, E.; Cardellach, F.; Miro, O.; Casademont, J. The effects of sepsis on mitochondria. J. Infect. Dis. 2012, 205, 392–400. [Google Scholar] [CrossRef] [PubMed]
- Kraft, B.D.; Chen, L.; Suliman, H.B.; Piantadosi, C.A.; Welty-Wolf, K.E. Peripheral blood mononuclear cells demonstrate mitochondrial damage clearance during sepsis. Crit. Care Med. 2019, 47, 651–658. [Google Scholar] [CrossRef] [PubMed]
- Kramer, P.A.; Ravi, S.; Chacko, B.; Johnson, M.S.; Darley-Usmar, V.M. A review of the mitochondrial and glycolytic metabolism in human platelets and leukocytes: Implications for their use as bioenergetic biomarkers. Redox Biol. 2014, 2, 206–210. [Google Scholar] [CrossRef] [PubMed]
- Zharikov, S.; Shiva, S. Platelet mitochondrial function: From regulation of thrombosis to biomarker of disease. Biochem. Soc. Trans. 2013, 41, 118–123. [Google Scholar] [CrossRef]
- Avila, C.; Huang, R.J.; Stevens, M.V.; Aponte, A.M.; Tripodi, D.; Kim, K.Y.; Sack, M.N. Platelet mitochondrial dysfunction is evident in type 2 diabetes in association with modifications of mitochondrial anti-oxidant stress proteins. Exp. Clin. Endocrinol. Diabetes 2012, 120, 248–251. [Google Scholar] [CrossRef]
- Sjovall, F.; Morota, S.; Hansson, M.J.; Friberg, H.; Gnaiger, E.; Elmer, E. Temporal increase of platelet mitochondrial respiration is negatively associated with clinical outcome in patients with sepsis. Crit. Care 2010, 14, R214. [Google Scholar] [CrossRef]
- Cardenes, N.; Corey, C.; Geary, L.; Jain, S.; Zharikov, S.; Barge, S.; Novelli, E.M.; Shiva, S. Platelet bioenergetic screen in sickle cell patients reveals mitochondrial complex V inhibition, which contributes to platelet activation. Blood 2014, 123, 2864–2872. [Google Scholar] [CrossRef]
- Chen, S.; Su, Y.; Wang, J. ROS-mediated platelet generation: A microenvironment-dependent manner for megakaryocyte proliferation, differentiation, and maturation. Cell Death Dis. 2013, 4, e722. [Google Scholar] [CrossRef]
- Maclay, J.D.; McAllister, D.A.; Johnston, S.; Raftis, J.; McGuinnes, C.; Deans, A.; Newby, D.E.; Mills, N.L.; MacNee, W. Increased platelet activation in patients with stable and acute exacerbation of COPD. Thorax 2011, 66, 769–774. [Google Scholar] [CrossRef]
- Bozza, F.A.; Shah, A.M.; Weyrich, A.S.; Zimmerman, G.A. Amicus or adversary: Platelets in lung biology, acute injury, and inflammation. Am. J. Respir. Cell Mol. Biol. 2009, 40, 123–134. [Google Scholar] [CrossRef]
- Chacko, B.K.; Kramer, P.A.; Ravi, S.; Johnson, M.S.; Hardy, R.W.; Ballinger, S.W.; Darley-Usmar, V.M. Methods for defining distinct bioenergetic profiles in platelets, lymphocytes, monocytes, and neutrophils, and the oxidative burst from human blood. Lab. Investig. 2013, 93, 690–700. [Google Scholar] [CrossRef] [PubMed]
- Al Amir Dache, Z.; Otandault, A.; Tanos, R.; Pastor, B.; Meddeb, R.; Sanchez, C.; Arena, G.; Lasorsa, L.; Bennett, A.; Grange, T.; et al. Blood contains circulating cell-free respiratory competent mitochondria. FASEB J. 2020. [Google Scholar] [CrossRef] [PubMed]
- Spinazzi, M.; Casarin, A.; Pertegato, V.; Salviati, L.; Angelini, C. Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat. Protoc. 2012, 7, 1235–1246. [Google Scholar] [CrossRef] [PubMed]
- Hsiao, C.-P.; Hoppel, C. Analyzing mitochondrial function in human peripheral blood mononuclear cells. Anal. Biochem. 2018, 549, 12–20. [Google Scholar] [CrossRef]
- Thannickal, V.J.; Fanburg, B.L. Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279, L1005–L1028. [Google Scholar] [CrossRef]
- Wallace, D.C. Diseases of the mitochondrial DNA. Annu. Rev. Biochem. 1992, 61, 1175–1212. [Google Scholar] [CrossRef]
- Aravamudan, B.; Thompson, M.A.; Pabelick, C.M.; Prakash, Y.S. Mitochondria in lung diseases. Expert Rev. Respir. Med. 2013, 7, 631–646. [Google Scholar] [CrossRef]
- Pan, S.; Conaway, S.J.; Deshpande, D.A. Mitochondrial regulation of airway smooth muscle functions in health and pulmonary diseases. Arch. Biochem. Biophys. 2019, 663, 109–119. [Google Scholar] [CrossRef]
- Prakash, Y.S.; Pabelick, C.M.; Sieck, G.C. Mitochondrial dysfunction in airway disease. Chest 2017, 152, 618–626. [Google Scholar] [CrossRef]
- Dikalov, S.; Itani, H.; Richmond, B.; Vergeade, A.; Rahman, S.M.J.; Boutaud, O.; Blackwell, T.; Massion, P.P.; Harrison, D.G.; Dikalova, A.; et al. Tobacco smoking induces cardiovascular mitochondrial oxidative stress, promotes endothelial dysfunction, and enhances hypertension. Am. J. Physiol. Heart Circ. Physiol. 2019, 316, H639–H646. [Google Scholar] [CrossRef]
- Wiegman, C.H.; Michaeloudes, C.; Haji, G.; Narang, P.; Clarke, C.J.; Russell, K.E.; Bao, W.; Pavlidis, S.; Barnes, P.J.; Kanerva, J.; et al. Oxidative stress-induced mitochondrial dysfunction drives inflammation and airway smooth muscle remodeling in patients with chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 2015, 136, 769–780. [Google Scholar] [CrossRef] [PubMed]
- Oka, T.; Hikoso, S.; Yamaguchi, O.; Taneike, M.; Takeda, T.; Tamai, T.; Oyabu, J.; Murakawa, T.; Nakayama, H.; Nishida, K.; et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012, 485, 251–255. [Google Scholar] [CrossRef] [PubMed]
- Caramori, G.; Casolari, P.; Barczyk, A.; Durham, A.L.; Di Stefano, A.; Adcock, I. COPD immunopathology. Semin. Immunopathol. 2016, 38, 497–515. [Google Scholar] [CrossRef] [PubMed]
- Comhair, S.A.A.; Erzurum, S.C. Antioxidant responses to oxidant-mediated lung diseases. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283, L246–L255. [Google Scholar] [CrossRef]
- MacNee, W. Oxidants and COPD. Curr. Drug Targets Inflamm. Allergy 2005, 4, 627–641. [Google Scholar] [CrossRef]
- Stevenson, C.S.; Koch, L.G.; Britton, S.L. Aerobic capacity, oxidant stress, and chronic obstructive pulmonary disease--a new take on an old hypothesis. Pharmacol. Ther. 2006, 110, 71–82. [Google Scholar] [CrossRef]
- Kovacic, P.; Somanathan, R. Pulmonary toxicity and environmental contamination: Radicals, electron transfer, and protection by antioxidants. Rev. Environ. Contam. Toxicol. 2009, 201, 41–69. [Google Scholar] [CrossRef]
- Colarusso, C.; Terlizzi, M.; Molino, A.; Pinto, A.; Sorrentino, R. Role of the inflammasome in chronic obstructive pulmonary disease (COPD). Oncotarget 2017, 8, 81813–81824. [Google Scholar] [CrossRef]
- De Falco, G.; Terlizzi, M.; Sirignano, M.; Commodo, M.; D’Anna, A.; Aquino, R.P.; Pinto, A.; Sorrentino, R. Human peripheral blood mononuclear cells (PBMCs) from smokers release higher levels of IL-1-like cytokines after exposure to combustion-generated ultrafine particles. Sci. Rep. 2017, 7, 43016. [Google Scholar] [CrossRef]
- Yang, W.; Ni, H.; Wang, H.; Gu, H. NLRP3 inflammasome is essential for the development of chronic obstructive pulmonary disease. Int. J. Clin. Exp. Pathol. 2015, 8, 13209–13216. [Google Scholar]
- Rahman, I.; Morrison, D.; Donaldson, K.; MacNee, W. Systemic oxidative stress in asthma, COPD, and smokers. Am. J. Respir. Crit. Care Med. 1996, 154, 1055–1060. [Google Scholar] [CrossRef] [PubMed]
- De Falco, G.; Colarusso, C.; Terlizzi, M.; Popolo, A.; Pecoraro, M.; Commodo, M.; Minutolo, P.; Sirignano, M.; D’Anna, A.; Aquino, R.P.; et al. Chronic obstructive pulmonary disease-derived circulating cells release IL-18 and. Front. Immunol. 2017, 8, 1415. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, A.R.; Kadam, S.; Brahme, A.; Agrawal, M.; Apte, K.; Narke, G.; Kekan, K.; Madas, S.; Salvi, S. Systemic Immuno-metabolic alterations in chronic obstructive pulmonary disease (COPD). Respir. Res. 2019, 20, 171. [Google Scholar] [CrossRef] [PubMed]
- Cheng, S.-C.; Scicluna, B.P.; Arts, R.J.W.; Gresnigt, M.S.; Lachmandas, E.; Giamarellos-Bourboulis, E.J.; Kox, M.; Manjeri, G.R.; Wagenaars, J.A.L.; Cremer, O.L.; et al. Broad defects in the energy metabolism of leukocytes underlie immunoparalysis in sepsis. Nat. Immunol. 2016, 17, 406–413. [Google Scholar] [CrossRef] [PubMed]
- Harrison, M.T.; Short, P.; Williamson, P.A.; Singanayagam, A.; Chalmers, J.D.; Schembri, S. Thrombocytosis is associated with increased short and long term mortality after exacerbation of chronic obstructive pulmonary disease: A role for antiplatelet therapy? Thorax 2014, 69, 609–615. [Google Scholar] [CrossRef]
- Bialas, A.J.; Pedone, C.; Piotrowski, W.J.; Antonelli Incalzi, R. Platelet distribution width as a prognostic factor in patients with COPD—Pilot study. Int. J. Chronic Obstr. Pulm. Dis. 2017, 12, 2261–2267. [Google Scholar] [CrossRef]
- Bialas, A.J.; Siewiera, K.; Watala, C.; Rybicka, A.; Grobelski, B.; Kosmider, L.; Kurek, J.; Milkowska-Dymanowska, J.; Piotrowski, W.J.; Gorski, P.; et al. Mitochondrial functioning abnormalities observed in blood platelets of chronic smoke-exposed guinea pigs-A pilot study. Int. J. Chronic Obstr. Pulm. Dis. 2018, 13, 3707–3717. [Google Scholar] [CrossRef]
- Salve, V.T.; Atram, J.S. N-Acetylcysteine combined with home based physical activity: Effect on health related quality of life in stable COPD patients—A Randomised controlled trial. J. Clin. Diagn. Res. 2016, 10, OC16–OC19. [Google Scholar] [CrossRef]
- Carpagnano, G.E.; Lacedonia, D.; Carone, M.; Soccio, P.; Cotugno, G.; Palmiotti, G.A.; Scioscia, G.; Foschino Barbaro, M.P. Study of mitochondrial DNA alteration in the exhaled breath condensate of patients affected by obstructive lung diseases. J. Breath Res. 2016, 10, 026005. [Google Scholar] [CrossRef]
- Zhang, W.Z.; Rice, M.C.; Hoffman, K.L.; Oromendia, C.; Barjaktarevic, I.; Wells, J.M.; Hastie, A.T.; Labaki, W.W.; Cooper, C.B.; Comellas, A.P.; et al. Association of urine mitochondrial DNA with clinical measures of COPD in the SPIROMICS cohort. JCI Insight 2020. [Google Scholar] [CrossRef]
- Liu, S.-F.; Kuo, H.-C.; Tseng, C.-W.; Huang, H.-T.; Chen, Y.-C.; Tseng, C.-C.; Lin, M.-C. Leukocyte Mitochondrial DNA Copy number is associated with chronic obstructive pulmonary disease. PLoS ONE 2015, 10, e0138716. [Google Scholar] [CrossRef] [PubMed]
- Carpagnano, G.E.; Lacedonia, D.; Malerba, M.; Palmiotti, G.A.; Cotugno, G.; Carone, M.; Foschino-Barbaro, M.P. Analysis of mitochondrial DNA alteration in new phenotype ACOS. BMC Pulm. Med. 2016, 16, 31. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.-H.; Kim, H.K.; Ko, J.-H.; Bang, H.; Lee, D.-C. The relationship between leukocyte mitochondrial DNA copy number and telomere length in community-dwelling elderly women. PLoS ONE 2013, 8, e67227. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.; Sandford, A.J.; Connett, J.E.; Yan, J.; Mui, T.; Li, Y.; Daley, D.; Anthonisen, N.R.; Brooks-Wilson, A.; Man, S.F.P.; et al. The relationship between telomere length and mortality in chronic obstructive pulmonary disease (COPD). PLoS ONE 2012, 7, e35567. [Google Scholar] [CrossRef]
- Jin, M.; Lee, E.C.; Ra, S.W.; Fishbane, N.; Tam, S.; Criner, G.J.; Woodruff, P.G.; Lazarus, S.C.; Albert, R.; Connett, J.E.; et al. Relationship of absolute telomere length with quality of life, exacerbations, and mortality in COPD. Chest 2018, 154, 266–273. [Google Scholar] [CrossRef]
- Pizzimenti, M.; Riou, M.; Charles, A.-L.; Talha, S.; Meyer, A.; Andres, E.; Chakfe, N.; Lejay, A.; Geny, B. The rise of mitochondria in peripheral arterial disease physiopathology: Experimental and clinical data. J. Clin. Med. 2019, 8. [Google Scholar] [CrossRef]
- Lambrecht, B.N.; Hammad, H. The immunology of asthma. Nat. Immunol. 2015, 16, 45–56. [Google Scholar] [CrossRef]
- Reddy, P.H. Mitochondrial dysfunction and oxidative stress in asthma: Implications for mitochondria-targeted antioxidant therapeutics. Pharmaceuticals 2011, 4, 429–456. [Google Scholar] [CrossRef]
- Aguilera-Aguirre, L.; Bacsi, A.; Saavedra-Molina, A.; Kurosky, A.; Sur, S.; Boldogh, I. Mitochondrial dysfunction increases allergic airway inflammation. J. Immunol. 2009, 183, 5379–5387. [Google Scholar] [CrossRef]
- Mabalirajan, U.; Dinda, A.K.; Kumar, S.; Roshan, R.; Gupta, P.; Sharma, S.K.; Ghosh, B. Mitochondrial structural changes and dysfunction are associated with experimental allergic asthma. J. Immunol. 2008, 181, 3540–3548. [Google Scholar] [CrossRef]
- Sahiner, U.M.; Birben, E.; Erzurum, S.; Sackesen, C.; Kalayci, O. Oxidative stress in asthma. World Allergy Organ. J. 2011, 4, 151–158. [Google Scholar] [CrossRef] [PubMed]
- Louhelainen, N.; Myllarniemi, M.; Rahman, I.; Kinnula, V.L. Airway biomarkers of the oxidant burden in asthma and chronic obstructive pulmonary disease: Current and future perspectives. Int. J. Chronic Obstr. Pulm. Dis. 2008, 3, 585–603. [Google Scholar]
- Comhair, S.A.A.; Ricci, K.S.; Arroliga, M.; Lara, A.R.; Dweik, R.A.; Song, W.; Hazen, S.L.; Bleecker, E.R.; Busse, W.W.; Chung, K.F.; et al. Correlation of systemic superoxide dismutase deficiency to airflow obstruction in asthma. Am. J. Respir. Crit. Care Med. 2005, 172, 306–313. [Google Scholar] [CrossRef] [PubMed]
- Chan, T.K.; Loh, X.Y.; Peh, H.Y.; Tan, W.N.F.; Tan, W.S.D.; Li, N.; Tay, I.J.J.; Wong, W.S.F.; Engelward, B.P. House dust mite-induced asthma causes oxidative damage and DNA double-strand breaks in the lungs. J. Allergy Clin. Immunol. 2016, 138, 84–96.e1. [Google Scholar] [CrossRef] [PubMed]
- Leffler, J.; Read, J.F.; Jones, A.C.; Mok, D.; Hollams, E.M.; Laing, I.A.; Le Souef, P.N.; Sly, P.D.; Kusel, M.M.H.; de Klerk, N.H.; et al. Progressive increase of FcepsilonRI expression across several PBMC subsets is associated with atopy and atopic asthma within school-aged children. Pediatr. Allergy Immunol. 2019, 30, 646–653. [Google Scholar] [CrossRef]
- Leffler, J.; Jones, A.C.; Hollams, E.M.; Prastanti, F.; Le Souef, P.N.; Holt, P.G.; Bosco, A.; Laing, I.A.; Strickland, D.H. Basophil counts in PBMC populations during childhood acute wheeze/asthma are associated with future exacerbations. J. Allergy Clin. Immunol. 2018, 142, 1639–1641.e5. [Google Scholar] [CrossRef]
- Ederle, C.; Charles, A.-L.; Khayath, N.; Poirot, A.; Meyer, A.; Clere-Jehl, R.; Andres, E.; De Blay, F.; Geny, B. Mitochondrial function in Peripheral Blood Mononuclear Cells (PBMC) is enhanced, together with increased reactive oxygen species, in severe asthmatic patients in exacerbation. J. Clin. Med. 2019, 8. [Google Scholar] [CrossRef]
- Clere-Jehl, R.; Helms, J.; Kassem, M.; Le Borgne, P.; Delabranche, X.; Charles, A.-L.; Geny, B.; Meziani, F.; Bilbault, P. Septic shock alters mitochondrial respiration of lymphoid cell-lines and human peripheral blood mononuclear cells: The role of plasma. Shock 2019, 51, 97–104. [Google Scholar] [CrossRef]
- Qi, S.; Barnig, C.; Charles, A.-L.; Poirot, A.; Meyer, A.; Clere-Jehl, R.; de Blay, F.; Geny, B. Effect of nasal allergen challenge in allergic rhinitis on mitochondrial function of peripheral blood mononuclear cells. Ann. Allergy Asthma Immunol. 2017, 118, 367–369. [Google Scholar] [CrossRef]
- Bhatraju, N.K.; Agrawal, A. Mitochondrial dysfunction linking obesity and asthma. Ann. Am. Thorac. Soc. 2017, 14, S368–S373. [Google Scholar] [CrossRef]
- Winnica, D.; Corey, C.; Mullett, S.; Reynolds, M.; Hill, G.; Wendell, S.; Que, L.; Holguin, F.; Shiva, S. Bioenergetic differences in the airway epithelium of lean versus obese asthmatics are driven by nitric oxide and reflected in circulating platelets. Antioxid. Redox Signal 2019, 31, 673–686. [Google Scholar] [CrossRef] [PubMed]
- Letuve, S.; Druilhe, A.; Grandsaigne, M.; Aubier, M.; Pretolani, M. Critical role of mitochondria, but not caspases, during glucocorticosteroid-induced human eosinophil apoptosis. Am. J. Respir. Cell Mol. Biol. 2002, 26, 565–571. [Google Scholar] [CrossRef] [PubMed]
- Idzko, M.; Pitchford, S.; Page, C. Role of platelets in allergic airway inflammation. J. Allergy Clin. Immunol. 2015, 135, 1416–1423. [Google Scholar] [CrossRef] [PubMed]
- Rondina, M.T.; Garraud, O. Emerging evidence for platelets as immune and inflammatory effector cells. Front. Immunol. 2014, 5, 653. [Google Scholar] [CrossRef] [PubMed]
- Averill, F.J.; Hubbard, W.C.; Proud, D.; Gleich, G.J.; Liu, M.C. Platelet activation in the lung after antigen challenge in a model of allergic asthma. Am. Rev. Respir. Dis. 1992, 145, 571–576. [Google Scholar] [CrossRef]
- Pitchford, S.C.; Momi, S.; Baglioni, S.; Casali, L.; Giannini, S.; Rossi, R.; Page, C.P.; Gresele, P. Allergen induces the migration of platelets to lung tissue in allergic asthma. Am. J. Respir. Crit. Care Med. 2008, 177, 604–612. [Google Scholar] [CrossRef]
- Gresele, P.; Dottorini, M.; Selli, M.L.; Iannacci, L.; Canino, S.; Todisco, T.; Romano, S.; Crook, P.; Page, C.P.; Nenci, G.G.; et al. Altered platelet function associated with the bronchial hyperresponsiveness accompanying nocturnal asthma. J. Allergy Clin. Immunol. 1993, 91, 894–902. [Google Scholar] [CrossRef]
- Kameyoshi, Y.; Dorschner, A.; Mallet, A.I.; Christophers, E.; Schroder, J.M. Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J. Exp. Med. 1992, 176, 587–592. [Google Scholar] [CrossRef]
- Klinger, M.H. Platelets and inflammation. Anat. Embryol. (Berl.) 1997, 196, 1–11. [Google Scholar] [CrossRef]
- Xu, W.; Cardenes, N.; Corey, C.; Erzurum, S.C.; Shiva, S. Platelets from asthmatic individuals show less reliance on glycolysis. PLoS ONE 2015, 10, e0132007. [Google Scholar] [CrossRef]
- Nguyen, Q.L.; Corey, C.; White, P.; Watson, A.; Gladwin, M.T.; Simon, M.A.; Shiva, S. Platelets from pulmonary hypertension patients show increased mitochondrial reserve capacity. JCI Insight 2017, 2, e91415. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, Q.L.; Wang, Y.; Helbling, N.; Simon, M.A.; Shiva, S. Alterations in platelet bioenergetics in Group 2 PH-HFpEF patients. PLoS ONE 2019, 14, e0220490. [Google Scholar] [CrossRef] [PubMed]
- Simonneau, G.; Montani, D.; Celermajer, D.S.; Denton, C.P.; Gatzoulis, M.A.; Krowka, M.; Williams, P.G.; Souza, R. Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur. Respir. J. 2019, 53. [Google Scholar] [CrossRef] [PubMed]
- Galie, N.; Humbert, M.; Vachiery, J.-L.; Gibbs, S.; Lang, I.; Torbicki, A.; Simonneau, G.; Peacock, A.; Vonk Noordegraaf, A.; Beghetti, M.; et al. 2015 ESC/ERS guidelines for the diagnosis and treatment of pulmonary hypertension: The joint task force for the diagnosis and treatment of pulmonary hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS): Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC), International Society for Heart and Lung Transplantation (ISHLT). Eur. Respir. J. 2015, 46, 903–975. [Google Scholar] [CrossRef] [PubMed]
- Kong, C.W.; Hsu, T.G.; Lu, F.J.; Chan, W.L.; Tsai, K. Leukocyte mitochondria depolarization and apoptosis in advanced heart failure: Clinical correlations and effect of therapy. J. Am. Coll. Cardiol. 2001, 38, 1693–1700. [Google Scholar] [CrossRef]
- Song, B.; Li, T.; Chen, S.; Yang, D.; Luo, L.; Wang, T.; Han, X.; Bai, L.; Ma, A. Correlations between MTP and ROS levels of peripheral blood lymphocytes and readmission in patients with chronic heart failure. Heart Lung Circ. 2016, 25, 296–302. [Google Scholar] [CrossRef]
- Kong, C.-W.; Huang, C.-H.; Hsu, T.-G.; Tsai, K.K.C.; Hsu, C.-F.; Huang, M.-C.; Chen, L.-C. Leukocyte mitochondrial alterations after cardiac surgery involving cardiopulmonary bypass: Clinical correlations. Shock 2004, 21, 315–319. [Google Scholar] [CrossRef]
- Humbert, M.; Guignabert, C.; Bonnet, S.; Dorfmuller, P.; Klinger, J.R.; Nicolls, M.R.; Olschewski, A.J.; Pullamsetti, S.S.; Schermuly, R.T.; Stenmark, K.R.; et al. Pathology and pathobiology of pulmonary hypertension: State of the art and research perspectives. Eur. Respir. J. 2019, 53. [Google Scholar] [CrossRef]
- Aggarwal, S.; Gross, C.M.; Sharma, S.; Fineman, J.R.; Black, S.M. Reactive oxygen species in pulmonary vascular remodeling. Compr. Physiol. 2013, 3, 1011–1034. [Google Scholar] [CrossRef]
- Bowers, R.; Cool, C.; Murphy, R.C.; Tuder, R.M.; Hopken, M.W.; Flores, S.C.; Voelkel, N.F. Oxidative stress in severe pulmonary hypertension. Am. J. Respir. Crit. Care Med. 2004, 169, 764–769. [Google Scholar] [CrossRef]
- Demarco, V.G.; Whaley-Connell, A.T.; Sowers, J.R.; Habibi, J.; Dellsperger, K.C. Contribution of oxidative stress to pulmonary arterial hypertension. World J. Cardiol. 2010, 2, 316–324. [Google Scholar] [CrossRef] [PubMed]
- Dorfmuller, P.; Chaumais, M.-C.; Giannakouli, M.; Durand-Gasselin, I.; Raymond, N.; Fadel, E.; Mercier, O.; Charlotte, F.; Montani, D.; Simonneau, G.; et al. Increased oxidative stress and severe arterial remodeling induced by permanent high-flow challenge in experimental pulmonary hypertension. Respir. Res. 2011, 12, 119. [Google Scholar] [CrossRef] [PubMed]
- Black, S.M.; DeVol, J.M.; Wedgwood, S. Regulation of fibroblast growth factor-2 expression in pulmonary arterial smooth muscle cells involves increased reactive oxygen species generation. Am. J. Physiol. Cell. Physiol. 2008, 294, C345–C354. [Google Scholar] [CrossRef] [PubMed]
- Dromparis, P.; Sutendra, G.; Michelakis, E.D. The role of mitochondria in pulmonary vascular remodeling. J. Mol. Med. (Berl.) 2010, 88, 1003–1010. [Google Scholar] [CrossRef]
- Dromparis, P.; Michelakis, E.D. Mitochondria in vascular health and disease. Annu. Rev. Physiol. 2013, 75, 95–126. [Google Scholar] [CrossRef]
- Gomez-Arroyo, J.; Mizuno, S.; Szczepanek, K.; Van Tassell, B.; Natarajan, R.; dos Remedios, C.G.; Drake, J.I.; Farkas, L.; Kraskauskas, D.; Wijesinghe, D.S.; et al. Metabolic gene remodeling and mitochondrial dysfunction in failing right ventricular hypertrophy secondary to pulmonary arterial hypertension. Circ. Heart Fail 2013, 6, 136–144. [Google Scholar] [CrossRef]
- Redout, E.M.; Wagner, M.J.; Zuidwijk, M.J.; Boer, C.; Musters, R.J.P.; van Hardeveld, C.; Paulus, W.J.; Simonides, W.S. Right-ventricular failure is associated with increased mitochondrial complex II activity and production of reactive oxygen species. Cardiovasc. Res. 2007, 75, 770–781. [Google Scholar] [CrossRef]
- Graham, B.B.; Kumar, R.; Mickael, C.; Sanders, L.; Gebreab, L.; Huber, K.M.; Perez, M.; Smith-Jones, P.; Serkova, N.J.; Tuder, R.M. Severe pulmonary hypertension is associated with altered right ventricle metabolic substrate uptake. Am. J. Physiol. Lung Cell. Mol. Physiol. 2015, 309, L435–L440. [Google Scholar] [CrossRef]
- Piao, L.; Marsboom, G.; Archer, S.L. Mitochondrial metabolic adaptation in right ventricular hypertrophy and failure. J. Mol. Med. (Berl.) 2010, 88, 1011–1020. [Google Scholar] [CrossRef]
- Malenfant, S.; Potus, F.; Fournier, F.; Breuils-Bonnet, S.; Pflieger, A.; Bourassa, S.; Tremblay, E.; Nehme, B.; Droit, A.; Bonnet, S.; et al. Skeletal muscle proteomic signature and metabolic impairment in pulmonary hypertension. J. Mol. Med. (Berl.) 2015, 93, 573–584. [Google Scholar] [CrossRef]
- Riou, M.; Pizzimenti, M.; Enache, I.; Charloux, A.; Canuet, M.; Andres, E.; Talha, S.; Meyer, A.; Geny, B. Skeletal and respiratory muscle dysfunctions in pulmonary arterial hypertension. J. Clin. Med. 2020, 9. [Google Scholar] [CrossRef] [PubMed]
- Diebold, I.; Hennigs, J.K.; Miyagawa, K.; Li, C.G.; Nickel, N.P.; Kaschwich, M.; Cao, A.; Wang, L.; Reddy, S.; Chen, P.-I.; et al. BMPR2 preserves mitochondrial function and DNA during reoxygenation to promote endothelial cell survival and reverse pulmonary hypertension. Cell Metab. 2015, 21, 596–608. [Google Scholar] [CrossRef] [PubMed]
- Chandel, N.S.; McClintock, D.S.; Feliciano, C.E.; Wood, T.M.; Melendez, J.A.; Rodriguez, A.M.; Schumacker, P.T. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: A mechanism of O2 sensing. J. Biol. Chem. 2000, 275, 25130–25138. [Google Scholar] [CrossRef] [PubMed]
- Block, K.; Gorin, Y.; Hoover, P.; Williams, P.; Chelmicki, T.; Clark, R.A.; Yoneda, T.; Abboud, H.E. NAD(P)H oxidases regulate HIF-2alpha protein expression. J. Biol. Chem. 2007, 282, 8019–8026. [Google Scholar] [CrossRef]
- Cheng, T.H.; Shih, N.L.; Chen, S.Y.; Loh, S.H.; Cheng, P.Y.; Tsai, C.S.; Liu, S.H.; Wang, D.L.; Chen, J.J. Reactive oxygen species mediate cyclic strain-induced endothelin-1 gene expression via Ras/Raf/extracellular signal-regulated kinase pathway in endothelial cells. J. Mol. Cell. Cardiol. 2001, 33, 1805–1814. [Google Scholar] [CrossRef]
- Tate, R.M.; Morris, H.G.; Schroeder, W.R.; Repine, J.E. Oxygen metabolites stimulate thromboxane production and vasoconstriction in isolated saline-perfused rabbit lungs. J. Clin. Investig. 1984, 74, 608–613. [Google Scholar] [CrossRef]
- Lee, D.S.; McCallum, E.A.; Olson, D.M. Effects of reactive oxygen species on prostacyclin production in perinatal rat lung cells. J. Appl. Physiol. (1985) 1989, 66, 1321–1327. [Google Scholar] [CrossRef]
- Chaumais, M.-C.; Ranchoux, B.; Montani, D.; Dorfmuller, P.; Tu, L.; Lecerf, F.; Raymond, N.; Guignabert, C.; Price, L.; Simonneau, G.; et al. N-acetylcysteine improves established monocrotaline-induced pulmonary hypertension in rats. Respir. Res. 2014, 15, 65. [Google Scholar] [CrossRef]
- Liu, M.; Wang, Y.; Zheng, L.; Zheng, W.; Dong, K.; Chen, S.; Zhang, B.; Li, Z. Fasudil reversed MCT-induced and chronic hypoxia-induced pulmonary hypertension by attenuating oxidative stress and inhibiting the expression of Trx1 and. Respir. Physiol. Neurobiol. 2014, 201, 38–46. [Google Scholar] [CrossRef]
- Mittal, M.; Roth, M.; Konig, P.; Hofmann, S.; Dony, E.; Goyal, P.; Selbitz, A.-C.; Schermuly, R.T.; Ghofrani, H.A.; Kwapiszewska, G.; et al. Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature. Circ. Res. 2007, 101, 258–267. [Google Scholar] [CrossRef]
- Vignais, P.V. The superoxide-generating NADPH oxidase: Structural aspects and activation mechanism. Cell. Mol. Life Sci. 2002, 59, 1428–1459. [Google Scholar] [CrossRef] [PubMed]
- Babior, B.M. The NADPH oxidase of endothelial cells. IUBMB Life 2000, 50, 267–269. [Google Scholar] [CrossRef]
- Cheng, Y.; Ren, X.; Gowda, A.S.P.; Shan, Y.; Zhang, L.; Yuan, Y.-S.; Patel, R.; Wu, H.; Huber-Keener, K.; Yang, J.W.; et al. Interaction of Sirt3 with OGG1 contributes to repair of mitochondrial DNA and protects from apoptotic cell death under oxidative stress. Cell Death Dis. 2013, 4, e731. [Google Scholar] [CrossRef] [PubMed]
- Paulin, R.; Dromparis, P.; Sutendra, G.; Gurtu, V.; Zervopoulos, S.; Bowers, L.; Haromy, A.; Webster, L.; Provencher, S.; Bonnet, S.; et al. Sirtuin 3 deficiency is associated with inhibited mitochondrial function and pulmonary arterial hypertension in rodents and humans. Cell Metab. 2014, 20, 827–839. [Google Scholar] [CrossRef] [PubMed]
- Zanjani, K.S. Platelets in pulmonary hypertension: A causative role or a simple association? Iran J. Pediatr. 2012, 22, 145–157. [Google Scholar]
- Johnson, S.R.; Granton, J.T.; Mehta, S. Thrombotic arteriopathy and anticoagulation in pulmonary hypertension. Chest 2006, 130, 545–552. [Google Scholar] [CrossRef]
- D’Souza, S.P.; Yellon, D.M.; Martin, C.; Schulz, R.; Heusch, G.; Onody, A.; Ferdinandy, P.; Baxter, G.F. B-type natriuretic peptide limits infarct size in rat isolated hearts via KATP channel opening. Am. J. Physiol. Heart Circ. Physiol. 2003, 284, H1592–H1600. [Google Scholar] [CrossRef]
- Talha, S.; Bouitbir, J.; Charles, A.-L.; Zoll, J.; Goette-Di Marco, P.; Meziani, F.; Piquard, F.; Geny, B. Pretreatment with brain natriuretic peptide reduces skeletal muscle mitochondrial dysfunction and oxidative stress after ischemia-reperfusion. J. Appl. Physiol. (1985) 2013, 114, 172–179. [Google Scholar] [CrossRef]
- Lederer, D.J.; Martinez, F.J. Idiopathic pulmonary fibrosis. N. Engl. J. Med. 2018, 378, 1811–1823. [Google Scholar] [CrossRef]
- Lopez-Otin, C.; Blasco, M.A.; Partridge, L.; Serrano, M.; Kroemer, G. The hallmarks of aging. Cell 2013, 153, 1194–1217. [Google Scholar] [CrossRef]
- Schafer, M.J.; White, T.A.; Iijima, K.; Haak, A.J.; Ligresti, G.; Atkinson, E.J.; Oberg, A.L.; Birch, J.; Salmonowicz, H.; Zhu, Y.; et al. Cellular senescence mediates fibrotic pulmonary disease. Nat. Commun. 2017, 8, 14532. [Google Scholar] [CrossRef] [PubMed]
- Negmadjanov, U.; Godic, Z.; Rizvi, F.; Emelyanova, L.; Ross, G.; Richards, J.; Holmuhamedov, E.L.; Jahangir, A. TGF-beta1-mediated differentiation of fibroblasts is associated with increased mitochondrial content and cellular respiration. PLoS ONE 2015, 10, e0123046. [Google Scholar] [CrossRef] [PubMed]
- Jain, M.; Rivera, S.; Monclus, E.A.; Synenki, L.; Zirk, A.; Eisenbart, J.; Feghali-Bostwick, C.; Mutlu, G.M.; Budinger, G.R.S.; Chandel, N.S.; et al. Mitochondrial reactive oxygen species regulate transforming growth factor-beta signaling. J. Biol. Chem. 2013, 288, 770–777. [Google Scholar] [CrossRef] [PubMed]
- Martinez, F.J.; de Andrade, J.A.; Anstrom, K.J.; King, T.E.J.; Raghu, G. Randomized trial of acetylcysteine in idiopathic pulmonary fibrosis. N. Engl. J. Med. 2014, 370, 2093–2101. [Google Scholar] [CrossRef]
- Heukels, P.; van Hulst, J.A.C.; van Nimwegen, M.; Boorsma, C.E.; Melgert, B.N.; van den Toorn, L.M.; Boomars, K.A.T.; Wijsenbeek, M.S.; Hoogsteden, H.; von der Thusen, J.H.; et al. Fibrocytes are increased in lung and peripheral blood of patients with idiopathic pulmonary fibrosis. Respir. Res. 2018, 19, 90. [Google Scholar] [CrossRef]
- Sode, B.F.; Dahl, M.; Nielsen, S.F.; Nordestgaard, B.G. Venous thromboembolism and risk of idiopathic interstitial pneumonia: A nationwide study. Am. J. Respir. Crit. Care Med. 2010, 181, 1085–1092. [Google Scholar] [CrossRef]
- Hubbard, R.B.; Smith, C.; Le Jeune, I.; Gribbin, J.; Fogarty, A.W. The association between idiopathic pulmonary fibrosis and vascular disease: A population-based study. Am. J. Respir. Crit. Care Med. 2008, 178, 1257–1261. [Google Scholar] [CrossRef]
- Leopold, J.A.; Maron, B.A. Molecular mechanisms of pulmonary vascular remodeling in pulmonary arterial hypertension. Int. J. Mol. Sci. 2016, 17. [Google Scholar] [CrossRef]
- Ryan, J.; Dasgupta, A.; Huston, J.; Chen, K.-H.; Archer, S.L. Mitochondrial dynamics in pulmonary arterial hypertension. J. Mol. Med. (Berl.) 2015, 93, 229–242. [Google Scholar] [CrossRef]
- Mizumura, K.; Cloonan, S.M.; Nakahira, K.; Bhashyam, A.R.; Cervo, M.; Kitada, T.; Glass, K.; Owen, C.A.; Mahmood, A.; Washko, G.R.; et al. Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD. J. Clin. Investig. 2014, 124, 3987–4003. [Google Scholar] [CrossRef]
- Ten, V.S.; Ratner, V. Mitochondrial bioenergetics and pulmonary dysfunction: Current progress and future directions. Paediatr. Respir. Rev. 2019. [Google Scholar] [CrossRef] [PubMed]
- Thannickal, V.J.; Toews, G.B.; White, E.S.; Lynch, J.P., 3rd; Martinez, F.J. Mechanisms of pulmonary fibrosis. Annu. Rev. Med. 2004, 55, 395–417. [Google Scholar] [CrossRef] [PubMed]
- Xie, N.; Tan, Z.; Banerjee, S.; Cui, H.; Ge, J.; Liu, R.-M.; Bernard, K.; Thannickal, V.J.; Liu, G. Glycolytic Reprogramming in Myofibroblast Differentiation and Lung Fibrosis. Am. J. Respir. Crit. Care Med. 2015, 192, 1462–1474. [Google Scholar] [CrossRef] [PubMed]
- Schuliga, M.; Pechkovsky, D.V.; Read, J.; Waters, D.W.; Blokland, K.E.C.; Reid, A.T.; Hogaboam, C.M.; Khalil, N.; Burgess, J.K.; Prele, C.M.; et al. Mitochondrial dysfunction contributes to the senescent phenotype of IPF lung fibroblasts. J. Cell. Mol. Med. 2018, 22, 5847–5861. [Google Scholar] [CrossRef] [PubMed]
- Manevski, M.; Muthumalage, T.; Devadoss, D.; Sundar, I.K.; Wang, Q.; Singh, K.P.; Unwalla, H.J.; Chand, H.S.; Rahman, I. Cellular stress responses and dysfunctional Mitochondrial-cellular senescence, and therapeutics in chronic respiratory diseases. Redox Biol. 2020, 101443. [Google Scholar] [CrossRef] [PubMed]
- Jablonski, R.P.; Kim, S.-J.; Cheresh, P.; Williams, D.B.; Morales-Nebreda, L.; Cheng, Y.; Yeldandi, A.; Bhorade, S.; Pardo, A.; Selman, M.; et al. SIRT3 deficiency promotes lung fibrosis by augmenting alveolar epithelial cell mitochondrial DNA damage and apoptosis. FASEB J. 2017, 31, 2520–2532. [Google Scholar] [CrossRef]
- Li, Y.; Ma, Y.; Song, L.; Yu, L.; Zhang, L.; Zhang, Y.; Xing, Y.; Yin, Y.; Ma, H. SIRT3 deficiency exacerbates p53/Parkinmediated mitophagy inhibition and promotes mitochondrial dysfunction: Implication for aged hearts. Int. J. Mol. Med. 2018, 41, 3517–3526. [Google Scholar] [CrossRef]
- Sanders, K.A.; Hoidal, J.R. The NOX on pulmonary hypertension. Circ. Res. 2007, 101, 224–226. [Google Scholar] [CrossRef]
- Chen, X.; Yao, J.-M.; Fang, X.; Zhang, C.; Yang, Y.-S.; Hu, C.-P.; Chen, Q.; Zhong, G.-W. Hypoxia promotes pulmonary vascular remodeling via HIF-1alpha to regulate mitochondrial dynamics. J. Geriatr. Cardiol. 2019, 16, 855–871. [Google Scholar] [CrossRef]
- Jaitovich, A.; Jourd’heuil, D. A brief overview of nitric oxide and reactive oxygen species signaling in hypoxia-induced pulmonary hypertension. Adv. Exp. Med. Biol. 2017, 967, 71–81. [Google Scholar] [CrossRef]
- Sun, T.; Liu, J.; Zhao, D.W. Efficacy of N-acetylcysteine in idiopathic pulmonary fibrosis: A systematic review and meta-analysis. Medicine (Baltimore) 2016, 95, e3629. [Google Scholar] [CrossRef] [PubMed]
- Sharp, J.; Farha, S.; Park, M.M.; Comhair, S.A.; Lundgrin, E.L.; Tang, W.H.W.; Bongard, R.D.; Merker, M.P.; Erzurum, S.C. Coenzyme Q supplementation in pulmonary arterial hypertension. Redox Biol. 2014, 2, 884–891. [Google Scholar] [CrossRef] [PubMed]
- Missiroli, S.; Genovese, I.; Perrone, M.; Vezzani, B.; Vitto, V.A.M.; Giorgi, C. The Role of mitochondria in inflammation: From cancer to neurodegenerative disorders. J. Clin. Med. 2020, 9. [Google Scholar] [CrossRef] [PubMed]
- Gu, X.; Wu, G.; Yao, Y.; Zeng, J.; Shi, D.; Lv, T.; Luo, L.; Song, Y. Intratracheal administration of mitochondrial DNA directly provokes lung inflammation through the TLR9-p38 MAPK pathway. Free Radic Biol. Med. 2015, 83, 149–158. [Google Scholar] [CrossRef] [PubMed]
- Benmerzoug, S.; Ryffel, B.; Togbe, D.; Quesniaux, V.F.J. Self-DNA Sensing in lung inflammatory diseases. Trends Immunol. 2019, 40, 719–734. [Google Scholar] [CrossRef]
References | Lung Disease Number of Patients | Type of Circulating Blood Cells | Mitochondrial Respiration | Oxidative Stress | mtDNA | Other Results |
---|---|---|---|---|---|---|
De Falco. 2017, Front Immunol [42] | Unstable COPD patients | PBMCs treated with combustion-generated ultrafine particles exposure | High level of mitochondrial dysfunction | High level of mtROS High expression of NOD-like receptor 3 in PBMCs in basal conditions in COPD patients | Release of cytokines: IL-18 and IL-33 (dependent on the release of caspase-4) | |
Bialas. 2018, Int J Chron Obstruct Pulmon Dis [47] | Chronic smoke-exposed guinea pig | Platelets | Increased proton and electron leak Decreased electron transfer system capacity | |||
Carpagnano. 2016, BMC Pulm Med [52] | ACOS patients (n = 23) COPD patients (n = 13) Asthmatic patients (n = 14) Normal subjects (n = 10) | PBMCs | Increased mtDNA/ nuclear DNA ratio in ACOS patients compared to other groups Increased mtDNA/ nuclear DNA in asthmatic or COPD patients compared to normal subjects | |||
Agarwal. 2019, Respir Res [43] | Tobacco smoke related COPD patients (n = 14) Non-smokers (n = 16) Healthy smokers (n = 13) | PBMCs | Impaired glucose metabolism in COPD subjects: lower OCR, ATP production, and spare respiratory capacity Impaired pyruvate metabolism in COPD subjects Impaired fatty acid metabolism in COPD subjects | Increase of inflammatory cytokine response (IFN-γ, IL-17, TNF-α, IL-5, IL-9, and IFN-α) | ||
Liu. 2015, PloS One [51] | COPD patients (n = 86) Healthy smokers (n = 33) Non-smokers (n = 77) | PBMCs | Decreased serum glutathione level in COPD | Decreased leukocyte mtDNA copy number of PBMCs in COPD Linear correlation between mtDNA copy number and serum glutathione level |
References | Lung Disease Number of Patients | Type of Circulating Blood Cells | Mitochondrial Respiration | Oxidative Stress | mtDNA | Other Results |
---|---|---|---|---|---|---|
Ederle. 2019, J Clin Med [67] | Severe asthmatic patients with severe exacerbation (n = 20) Healthy volunteers (n = 20) | PBMCs | Increased PBMCs mitochondrial respiratory chain complexes activity in asthmatic patients Mitochondrial respiratory chain complexes activity in PBMCs is related to plasma constituent | Increased ROS production in the blood of asthmatic patients ROS production is related to plasma constituent | ||
Winnica. 2019, Antiox Redox Signal [71] | Lean and obese, mild to moderate, asthmatic patients (n = 16) Lean and obese healthy volunteers (n = 21) | Platelets | Similar basal OCR in lean healthy and asthmatic subjects Increased basal OCR in asthmatic obese Enhanced maximal OCR in lean and obese asthmatic patients | Enhanced ROS production in lean and obese asthmatics | ||
Xu. 2015, Plos One. [80] | Asthmatic patients (n = 12) Healthy controls (n = 13) | Platelets | Similar OCR in both groups Decreased glycolytic rate and greater tricarboxylic acid cycle activity in asthmatic platelets | No change in mtDNA content | No change in mitochondrial number and morphology | |
Nguyen. 2017, JCI Insight [81] | Group 1 PAH patients (n = 28) Control patients (n = 28) | Platelets | Increased glycolytic rate in PAH patients: decrease of pyruvate dehydrogenase activity No change in basal respiration Enhanced respiratory reserve capacity in PAH dependent on increased fatty acid oxidation Increase in complex II enzymatic activity and decrease in complex I enzymatic activity. No change in enzymatic activity of complex IV. | No change in mitochondrial superoxide production | Positive correlation between respiratory reserve capacity and hemodynamic severity (mean PAP, PVR and right ventricle stroke work index) No change following phosphodiesterase 5 inhibitions, prostacyclin analogue and endothelin receptor antagonist | |
Nguyen. 2019, Plos one. [82] | Group 2 PH patients (n = 20) Control patients (n = 20) | Platelets | No significant difference in basal oxygen consumption rate. Increased maximal oxygen consumption rate (increased contribution of fatty acid and glucose oxidation). | No difference in mitochondrial superoxide production. | Negative correlation between maximal mitochondrial respiration and right ventricular stroke work index No change following nitrite inhalation. |
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Riou, M.; Alfatni, A.; Charles, A.-L.; Andrès, E.; Pistea, C.; Charloux, A.; Geny, B. New Insights into the Implication of Mitochondrial Dysfunction in Tissue, Peripheral Blood Mononuclear Cells, and Platelets during Lung Diseases. J. Clin. Med. 2020, 9, 1253. https://doi.org/10.3390/jcm9051253
Riou M, Alfatni A, Charles A-L, Andrès E, Pistea C, Charloux A, Geny B. New Insights into the Implication of Mitochondrial Dysfunction in Tissue, Peripheral Blood Mononuclear Cells, and Platelets during Lung Diseases. Journal of Clinical Medicine. 2020; 9(5):1253. https://doi.org/10.3390/jcm9051253
Chicago/Turabian StyleRiou, Marianne, Abrar Alfatni, Anne-Laure Charles, Emmanuel Andrès, Cristina Pistea, Anne Charloux, and Bernard Geny. 2020. "New Insights into the Implication of Mitochondrial Dysfunction in Tissue, Peripheral Blood Mononuclear Cells, and Platelets during Lung Diseases" Journal of Clinical Medicine 9, no. 5: 1253. https://doi.org/10.3390/jcm9051253
APA StyleRiou, M., Alfatni, A., Charles, A.-L., Andrès, E., Pistea, C., Charloux, A., & Geny, B. (2020). New Insights into the Implication of Mitochondrial Dysfunction in Tissue, Peripheral Blood Mononuclear Cells, and Platelets during Lung Diseases. Journal of Clinical Medicine, 9(5), 1253. https://doi.org/10.3390/jcm9051253