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Pericytes and Smooth Muscle Cells Circulating in the Blood as Markers of Impaired Angiogenesis during Combined Metabolic Impairments and Lung Emphysema

The changes in endothelial progenitor cells and progenitor cells of angiogenesis, pericytes and smooth muscle cells, were studied in female C57BL/6 mice with a combination of metabolic impairments induced by injections of sodium glutamate and lung emphysema modeled by the administration of cigarette smoke extract. It was observed that sodium glutamate significantly enhances pathological changes in the lungs (inflammation and lung emphysema) induced by the administration of cigarette smoke extract. Recruiting of endothelial progenitor cells (CD45CD31+CD34+ and CD31+CD34+CD146) and progenitor cells of angiogenesis (CD45CD117+CD309+) was registered in the injured lungs. Angiogenesis impairment induced by combined exposure is related to altered migration of pericytes (CD31CD34CD146+) and smooth muscle cells (CD31CD34+CD146+) in emphysema-like enlarged lung tissue.

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  1. 1.

    Chuchalin AG, Tseimakh I Ya, Momot AP, Mamaev AN, Karbyshev IA, Kostyuchenko GI. Changes in systemic inflammatory and hemostatic reactions in patients with exacerbation of chronic obstructive pulmonary disease with concomitant chronic heart failure and obesity. Pul’monologiya. 2014;(6):25-32. Russian.

  2. 2.

    Agustí A, Barberà JA, Wouters EF, Peinado VI, Jeffery PK. Lungs, bone marrow, and adipose tissue. A network approach to the pathobiology of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2013;188(12):1396-1406.

    Google Scholar 

  3. 3.

    Ambasta RK, Kohli H, Kumar P. Multiple therapeutic effect of endothelial progenitor cell regulated by drugs in diabetes and diabetes related disorder. J. Transl. Med. 2017;15(1):185. doi:

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Cameron DP, Poon TK, Smith GC. Effects of monosodium glutamate administration in the neonatal period on the diabetic syndrome in KK mice. Diabetologia. 1976;12(6):621-626.

    CAS  Article  Google Scholar 

  5. 5.

    Díez-Manglano J, Barquero-Romero J, Almagro P, Cabrera FJ, López García F, Montero L, Soriano JB; Working Group on COPD; Spanish Society of Internal Medicine. COPD patients with and without metabolic syndrome: clinical and functional differences. Intern. Emerg. Med. 2014;9(4):419-425.

    Google Scholar 

  6. 6.

    Doyle MF, Tracy RP, Parikh MA, Hoffman EA, Shimbo D, Austin JH, Smith BM, Hueper K, Vogel-Claussen J, Lima J, Gomes A, Watson K, Kawut S, Barr RG. Endothelial progenitor cells in chronic obstructive pulmonary disease and emphysema. PLoS One. 2017;12(3. ID e0173446. doi:

    Article  Google Scholar 

  7. 7.

    García-Rio F, Soriano JB, Miravitlles M, Muñoz L, Duran-Tauleria E, Sánchez G, Sobradillo V, Ancochea J. Impact of obesity on the clinical profile of a population-based sample with chronic obstructive pulmonary disease. PLoS One. 2014;9(8). ID e105220. doi:

    Article  Google Scholar 

  8. 8.

    Hanson C, LeVan T. Obesity and chronic obstructive pulmonary disease: recent knowledge and future directions. Curr. Opin. Pulm. Med. 2017;23(2):149-153.

    Article  Google Scholar 

  9. 9.

    Lamonaca P, Prinzi G, Kisialiou A, Cardaci V, Fini M, Russo P. Metabolic disorder in Chronic Obstructive Pulmonary Disease (COPD) patients: towards a personalized approach using marine drug derivatives. Mar. Drugs. 2017;15(3). pii: E81. doi:

    Article  Google Scholar 

  10. 10.

    Matsushita K, Dzau VJ. Mesenchymal stem cells in obesity: insights for translational applications. Lab. Invest. 2017;97(10):1158-1166.

    Article  Google Scholar 

  11. 11.

    Matysková R, Maletínská L, Maixnerová J, Pirník Z, Kiss A, Zelezná B. Comparison of the obesity phenotypes related to monosodium glutamate effect on arcuate nucleus and/or the high fat diet feeding in C57BL/6 and NMRI mice. Physiol. Res. 2008;57(5):727-734.

    PubMed  Google Scholar 

  12. 12.

    Miller J, Edwards LD, Agustí A, Bakke P, Calverley PM, Celli B, Coxson HO, Crim C, Lomas DA, Miller BE, Rennard S, Silverman EK, Tal-Singer R, Vestbo J, Wouters E, Yates JC, Macnee W; Evaluation of COPD Longitudinally to Identify Predictive Surrogate Endpoints (ECLIPSE) Investigators. Comorbidity, systemic inflammation and outcomes in the ECLIPSE cohort. Respir. Med. 2013;107(9):1376-1384.

    Google Scholar 

  13. 13.

    Nusaiba S, Fatima SA, Hussaini G, Mikail HG. Anaemogenic, obesogenic and thermogenic potentials of graded doses of monosodium glutamate sub-acutely fed to experimental Wistar rats. Curr. Clin. Pharmacol. 2018;13(4):273-278.

    Article  Google Scholar 

  14. 14.

    Sasaki Y, Suzuki W, Shimada T, Iizuka S, Nakamura S, Nagata M, Fujimoto M, Tsuneyama K, Hokao R, Miyamoto K, Aburada M. Dose dependent development of diabetes mellitus and non-alcoholic steatohepatitis in monosodium glutamateinduced obese mice. Life Sci. 2009;85(13-14):490-498.

    CAS  Article  Google Scholar 

  15. 15.

    Skurikhin EG, Pershina OV, Pakhomova AV, Pan ES, Krupin VA, Ermakova NN, Vaizova OE, Pozdeeva AS, Zhukova MA, Skurikhina VE, Grimm WD, Dygai AM. Endothelial progenitor cells as pathogenetic and diagnostic factors, and potential targets for GLP-1 in combination with metabolic syndrome and chronic obstructive pulmonary disease. Int. J. Mol. Sci. 2019;20(5). pii: E1105. doi:

    CAS  Article  Google Scholar 

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Correspondence to E. G. Skurikhin.

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Translated from Byulleten’ Eksperimental’noi Biologii i Meditsiny, Vol, 168, No, 9, pp. 301-307, September, 2019

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Pakhomova, A.V., Pershina, O.V., Ermakova, N.N. et al. Pericytes and Smooth Muscle Cells Circulating in the Blood as Markers of Impaired Angiogenesis during Combined Metabolic Impairments and Lung Emphysema. Bull Exp Biol Med 168, 334–340 (2020).

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Key Words

  • metabolic impairments
  • lung emphysema
  • endothelial progenitor cells
  • pericytes
  • smooth muscle cells