Anat Cell Biol.  2024 Mar;57(1):105-118. 10.5115/acb.23.217.

Impact of peripheral blood mononuclear cells preconditioned by activated platelet supernatant in managing gastric mucosal damage induced by zinc oxide nanoparticles in rats

Affiliations
  • 1Department of Anatomy and Histology, Faculty of Medicine, the University of Jordan and Ibn Sina University for Medical Sciences, Amman, Jordan
  • 2Department of Basic Medical Sciences, Faculty of Medicine, Ibn Sina University for Medical Sciences, Amman, Jordan
  • 3Department of Histology and Cell Biology, Faculty of Medicine, Tanta University, Tanta, Egypt
  • 4Department of Human Anatomy and Embryology, Faculty of Medicine, Mansoura University, Mansoura, Egypt
  • 5Department of Physiology, Faculty of Medicine, Mansoura University, Mansoura, Egypt

Abstract

The world has witnessed tremendous advancements in nano-base applications. Zinc oxide nanoparticles (ZON) are widely used in food industry and medicine. Although their application is of important value, they may cause toxicity to body tissues. Peripheral blood mononuclear cells (PBMCs) proved its efficacy in tissue regeneration especially when it is preconditioned by activated platelet supernatant (APS). The aim of this study is to evaluate the effect of ZON on the gastric mucosa and the therapeutic role of the PBMCs preconditioned by APS in rats. Ten rats were donors and fifty rats were recipients. The recipients were divided into; control group, ZON group (10 mg/kg/day orally for five days) and preconditioned PBMCs group (1×107 once intravenously 24 hours after ZON). Gastric specimens were processed for histological, immunohistochemical, biochemical and quantitative real-time polymerase chain reaction studies. ZON group showed marked structural changes in the gastric mucosa. There was desquamation or deep ulceration of the epithelium. Cytoplasmic vacuoles and pyknotic nuclei were in glandular cells. Reduced proliferating cell nuclear antigen and increased tumor necrosis factor-α were in epithelial cells. There were significant elevation in malondialdahyde and reduction in glutathione, superoxide dismutase, and catalase. Enhancement in mRNA expression of nuclear factor kappa-B and cyclooxygenase-2 was detected. The preconditioned PBMCs group showed significant improvement of all parameters. So, ZON had cytotoxic effects on the gastric mucosa and the preconditioned PBMCs had a therapeutic effect on gastric mucosal damage after ZON.

Keyword

Leukocytes; mononuclear; Activated platelet supernatant; Zinc oxide nanoparticles; Gastric mucosa

Figure

  • Fig. 1 Transmission electron microscopic analysis of ZON.

  • Fig. 2 Representative photomicrographs of H&E stained section of group I showing: (A) The fundic mucosa with smooth epithelial surface (arrows), lamina propria (*) and muscularis mucosa (M). Notice the simple tubular glands (G) and lymphoid cells (L) in the lamina propria. (B) The surface and pits lined by simple columnar cells with oval nuclei and pale acidophilic cytoplasm (arrows). The underlying lamina propria contains blood vessels and smooth muscle cells (*). Notice acidophilic parietal cells (arrow heads) predominating in the upper part of the glands. (C) The darker chief cells (arrow heads) predominating in the basal part of the glands. Notice the blood vessels, lymphoid cells and smooth muscle cells of the lamina propria (*). (A) Magnification ×100, (B, C) ×400.

  • Fig. 3 Representative photomicrographs of H&E stained section of group II showing: (A) Sloughing and desquamation of the surface epithelium (arrows). (B) Deep ulceration of the epithelium extending to muscularis mucosa (arrow). Notice reduced cytoplasmic acidophilia of some parietal cells (arrow heads). (C) Reduced acidophilia, cytoplasmic vacuolation (arrows) and deeply stained pyknotic nuclei (arrow heads) of the parietal cells. (D) Shrunken cells in the basal part of the glands with deeply stained pyknotic nuclei (arrow heads). Notice markedly dilated congested blood vessels (*). (A) Magnification ×100, (B–D) ×400.

  • Fig. 4 Representative photomicrographs of H&E stained section of group III showing: (A) The fundic mucosa with smooth epithelial surface (arrows). Notice closely packed simple tubular glands (G) in the lamina propria. (B) The surface and pits lined by simple columnar mucous cells with oval nuclei (arrows). (C) Closely packed glands with nearly intact lining cells (G) and a few dilated blood vessels were observed in the lamina propria (*). Notice a few vacuolated or shrunken glandular cells (arrow heads). (A) Magnification ×100, (B, C) ×400.

  • Fig. 5 Representative photomicrographs of proliferating cell nuclear antigen (PCNA) immunostained sections; (A) Group I shows intense PCNA reaction in the nuclei of many epithelial cells in the neck of the fundic glands (arrows). (B) Group II shows reduced PCNA positive cells with very weak PCNA nuclear expression in most epithelial cells (arrows). (C) Group III shows moderate PCNA nuclear expression in many epithelial cells (arrows). (A–C) Magnification ×400.

  • Fig. 6 Representative photomicrographs of tumor necrosis factor-α (TNF-α) immunostained sections; (A) Group I shows weak TNF-α immunoreaction in the cytoplasm of a few epithelial cells of the fundic glands (arrows). (B) Group II shows strong TNF-α cytoplasmic immunoreaction in many epithelial cells (arrows). (C) Group III shows moderate TNF-α cytoplasmic immunoreaction in some epithelial cells (arrows). (A–C) Magnification ×400.

  • Fig. 7 Morphometrical and statistical analysis of proliferating cell nuclear antigen (PCNA) mean area %.

  • Fig. 8 Morphometrical and statistical analysis of tumor necrosis factor-α (TNF-α) mean area %.

  • Fig. 9 mRNA expression of nuclear factor kappa-B (NF-ĸB) and cyclooxygenase-2 (COX-2).


Reference

References

1. Islam F, Shohag S, Uddin MJ, Islam MR, Nafady MH, Akter A, Mitra S, Roy A, Emran TB, Cavalu S. 2022; Exploring the journey of zinc oxide nanoparticles (ZnO-NPs) toward biomedical applications. Materials (Basel). 15:2160. DOI: 10.3390/ma15062160. PMID: 35329610. PMCID: PMC8951444.
Article
2. Alotaibi B, Negm WA, Elekhnawy E, El-Masry TA, Elharty ME, Saleh A, Abdelkader DH, Mokhtar FA. 2022; Antibacterial activity of nano zinc oxide green-synthesised from Gardenia thailandica triveng. Leaves against Pseudomonas aeruginosa clinical isolates: in vitro and in vivo study. Artif Cells Nanomed Biotechnol. 50:96–106. DOI: 10.1080/21691401.2022.2056191. PMID: 35361019.
Article
3. Motelica L, Oprea OC, Vasile BS, Ficai A, Ficai D, Andronescu E, Holban AM. 2023; Antibacterial activity of solvothermal obtained ZnO nanoparticles with different morphology and photocatalytic activity against a dye mixture: methylene blue, rhodamine B and methyl orange. Int J Mol Sci. 24:5677. DOI: 10.3390/ijms24065677. PMID: 36982751. PMCID: PMC10058279.
Article
4. Anjum S, Hashim M, Malik SA, Khan M, Lorenzo JM, Abbasi BH, Hano C. 2021; Recent advances in zinc oxide nanoparticles (ZnO NPs) for cancer diagnosis, target drug delivery, and treatment. Cancers (Basel). 13:4570. DOI: 10.3390/cancers13184570. PMID: 34572797. PMCID: PMC8468934.
Article
5. Hu C, Du W. 2020; Zinc oxide nanoparticles (ZnO NPs) combined with cisplatin and gemcitabine inhibits tumor activity of NSCLC cells. Aging (Albany NY). 12:25767–77. DOI: 10.18632/aging.104187. PMID: 33232271. PMCID: PMC7803530.
Article
6. Abdelkader DH, Negm WA, Elekhnawy E, Eliwa D, Aldosari BN, Almurshedi AS. 2022; Zinc oxide nanoparticles as potential delivery carrier: green synthesis by Aspergillus niger endophytic fungus, characterization, and in vitro/in vivo antibacterial activity. Pharmaceuticals (Basel). 15:1057. DOI: 10.3390/ph15091057. PMID: 36145278. PMCID: PMC9500724.
Article
7. Kuhlbusch TAJ, Wijnhoven SWP, Haase A. 2018; Nanomaterial exposures for worker, consumer and the general public. Nanoimpact. 1:11–25. DOI: 10.1016/j.impact.2017.11.003.
Article
8. Mendoza-Milla C, Macías Macías FI, Velázquez Delgado KA, Herrera Rodríguez MA, Colín-Val Z, Ramos-Godinez MDP, Cano-Martínez A, Vega-Miranda A, Robledo-Cadena DX, Delgado-Buenrostro NL, Chirino YI, Flores-Flores JO, López-Marure R. 2022; Zinc oxide nanoparticles induce toxicity in H9c2 rat cardiomyoblasts. Int J Mol Sci. 23:12940. DOI: 10.3390/ijms232112940. PMID: 36361726. PMCID: PMC9658273.
Article
9. Almansour MI, Alferah MA, Shraideh ZA, Jarrar BM. 2017; Zinc oxide nanoparticles hepatotoxicity: histological and histochemical study. Environ Toxicol Pharmacol. 51:124–30. DOI: 10.1016/j.etap.2017.02.015. PMID: 28236584.
Article
10. Dkhil MA, Diab MSM, Aljawdah HMA, Murshed M, Hafiz TA, Al-Quraishy S, Bauomy AA. 2020; Neuro-biochemical changes induced by zinc oxide nanoparticles. Saudi J Biol Sci. 27:2863–7. DOI: 10.1016/j.sjbs.2020.07.009. PMID: 32994747. PMCID: PMC7499291.
Article
11. Rafiee Z, Khorsandi L, Nejad-Dehbashi F. 2019; Protective effect of Zingerone against mouse testicular damage induced by zinc oxide nanoparticles. Environ Sci Pollut Res Int. 26:25814–24. DOI: 10.1007/s11356-019-05818-3. PMID: 31270769.
Article
12. Pinho AR, Rebelo S, Pereira ML. 2020; The impact of zinc oxide nanoparticles on male (in)fertility. Materials (Basel). 13:849. DOI: 10.3390/ma13040849. PMID: 32069903. PMCID: PMC7078810.
Article
13. Mohammed HAL, El Shakaa NM, Bahaa N, Zeid AAA. 2021; A histological study on the acute effect of zinc oxide nanoparticles administered by different routes on albino rat lung. J Microsc Ultrastruct. 10:72–80. DOI: 10.4103/jmau.jmau_114_20. PMID: 35832310. PMCID: PMC9272692.
Article
14. Mawed SA, Marini C, Alagawany M, Farag MR, Reda RM, El-Saadony MT, Elhady WM, Magi GE, Di Cerbo A, El-Nagar WG. 2022; Zinc oxide nanoparticles (ZnO-NPs) suppress fertility by activating autophagy, apoptosis, and oxidative stress in the developing oocytes of female zebrafish. Antioxidants (Basel). 11:1567. DOI: 10.3390/antiox11081567. PMID: 36009286. PMCID: PMC9404823.
Article
15. Ramadan AG, Yassein AAM, Eissa EA, Mahmoud MS, Hassan GM. 2022; Biochemical and histopathological alterations induced by subchronic exposure to zinc oxide nanoparticle in male rats and assessment of its genotoxicicty. J Umm Al-Qura Univ Appl Sci. 8:41–9. DOI: 10.1007/s43994-022-00008-3.
Article
16. Li Y, Li F, Zhang L, Zhang C, Peng H, Lan F, Peng S, Liu C, Guo J. 2020; Zinc oxide nanoparticles induce mitochondrial biogenesis impairment and cardiac dysfunction in human iPSC-derived cardiomyocytes. Int J Nanomedicine. 15:2669–83. DOI: 10.2147/IJN.S249912. PMID: 32368048. PMCID: PMC7183345.
17. Xia T, Kovochich M, Liong M, Mädler L, Gilbert B, Shi H, Yeh JI, Zink JI, Nel AE. 2008; Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano. 2:2121–34. Erratum in: ACS Nano 2008;2:2592. DOI: 10.1021/nn800511k. PMID: 19206459. PMCID: PMC3959800.
Article
18. Liu Z, Lv X, Xu L, Liu X, Zhu X, Song E, Song Y. 2020; Zinc oxide nanoparticles effectively regulate autophagic cell death by activating autophagosome formation and interfering with their maturation. Part Fibre Toxicol. 17:46. DOI: 10.1186/s12989-020-00379-7. PMID: 32948194. PMCID: PMC7501661.
Article
19. Feng Y, Min L, Zhang W, Liu J, Hou Z, Chu M, Li L, Shen W, Zhao Y, Zhang H. 2017; Zinc oxide nanoparticles influence microflora in ileal digesta and correlate well with blood metabolites. Front Microbiol. 8:992. DOI: 10.3389/fmicb.2017.00992. PMID: 28626453. PMCID: PMC5454036.
Article
20. Youn SM, Choi SJ. 2022; Food additive zinc oxide nanoparticles: dissolution, interaction, fate, cytotoxicity, and oral toxicity. Int J Mol Sci. 23:6074. DOI: 10.3390/ijms23116074. PMID: 35682753. PMCID: PMC9181433.
Article
21. Liao C, Jin Y, Li Y, Tjong SC. 2020; Interactions of zinc oxide nanostructures with mammalian cells: cytotoxicity and photocatalytic toxicity. Int J Mol Sci. 21:6305. DOI: 10.3390/ijms21176305. PMID: 32878253. PMCID: PMC7504403.
Article
22. Chang YN, Zhang M, Xia L, Zhang J, Xing G. 2012; The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials (Basel). 5:2850–71. DOI: 10.3390/ma5122850. PMCID: PMC5449046.
Article
23. Kim YR, Park JI, Lee EJ, Park SH, Seong NW, Kim JH, Kim GY, Meang EH, Hong JS, Kim SH, Koh SB, Kim MS, Kim CS, Kim SK, Son SW, Seo YR, Kang BH, Han BS, An SS, Yun HI, Kim MK. 2014; Toxicity of 100 nm zinc oxide nanoparticles: a report of 90-day repeated oral administration in Sprague Dawley rats. Int J Nanomedicine. 9 Suppl 2:109–26. DOI: 10.2147/IJN.S57928. PMID: 25565830. PMCID: PMC4279774.
24. Abdallah EAA, Omran BHF, Abdelwahab MM. 2018; A study of subchronic genotoxic effects of zinc oxide nanoparticles and protective role of vitamin E on the stomach and pancreas in adult albino rats. Egypt J Forensic Sci Appl Toxicol. 18:25–41. DOI: 10.21608/ejfsat.2018.4194.1017.
25. Hoang DM, Pham PT, Bach TQ, Ngo ATL, Nguyen QT, Phan TTK, Nguyen GH, Le PTT, Hoang VT, Forsyth NR, Heke M, Nguyen LT. 2022; Stem cell-based therapy for human diseases. Signal Transduct Target Ther. 7:272. DOI: 10.1038/s41392-022-01134-4. PMID: 35933430. PMCID: PMC9357075.
Article
26. El-Kadiry AE, Rafei M, Shammaa R. 2021; Cell therapy: types, regulation, and clinical benefits. Front Med (Lausanne). 8:756029. DOI: 10.3389/fmed.2021.756029. PMID: 34881261. PMCID: PMC8645794.
Article
27. Abo-Elyazed AA, Kassab AA, Elbakary NAM, Abo-Raya AA, Shalaby NM. The therapeutic effect of activated platelet supernatant-primed mobilized peripheral blood mononuclear cells on experimentally induced ulcers in the ileum of of adult male albino rat: histological and immunohistochemical study. Egypt J Histol. 2022; [In press]. DOI: 10.21608/ejh.2022.155155.1749.
28. Sen P, Kemppainen E, Orešič M. 2018; Perspectives on systems modeling of human peripheral blood mononuclear cells. Front Mol Biosci. 4:96. DOI: 10.3389/fmolb.2017.00096. PMID: 29376056. PMCID: PMC5767226.
Article
29. Supartono B, Farida S, Suhandono S, Yusuf AA. 2022; Safety evaluation of human peripheral blood mononuclear cells in naive rats:a chronic toxicity study. Bangladesh J Med Sci. 21:373–83. DOI: 10.3329/bjms.v21i2.57029.
Article
30. Sarasúa JG, López SP, Viejo MA, Basterrechea MP, Rodríguez AF, Gutiérrez AF, Gala JG, Menéndez YM, Augusto DE, Arias AP, Hernández JO. 2011; Treatment of pressure ulcers with autologous bone marrow nuclear cells in patients with spinal cord injury. J Spinal Cord Med. 34:301–7. DOI: 10.1179/2045772311Y.0000000010. PMID: 21756569. PMCID: PMC3127373.
Article
31. Zhang J, Zhai H, Yu P, Shang D, Mo R, Li Z, Wang X, Lu J, Xie Q, Xiang X. 2022; Human umbilical cord blood mononuclear cells ameliorate CCl4-induced acute liver injury in mice via inhibiting inflammatory responses and upregulating peripheral interleukin-22. Front Pharmacol. 13:924464. DOI: 10.3389/fphar.2022.924464. PMID: 35942221. PMCID: PMC9356225.
Article
32. Tanaka R, Fujimura S, Kado M, Fukuta T, Arita K, Hirano-Ito R, Mita T, Watada H, Kato Y, Miyauchi K, Mizuno H. 2022; Phase I/IIa feasibility trial of autologous quality- and quantity-cultured peripheral blood mononuclear cell therapy for non-healing extremity ulcers. Stem Cells Transl Med. 11:146–58. DOI: 10.1093/stcltm/szab018. PMID: 35298656. PMCID: PMC8929435.
Article
33. Hatakeyama M, Kanazawa M, Ninomiya I, Omae K, Kimura Y, Takahashi T, Onodera O, Fukushima M, Shimohata T. 2019; A novel therapeutic approach using peripheral blood mononuclear cells preconditioned by oxygen-glucose deprivation. Sci Rep. 9:16819. Erratum in: Sci Rep 2019;9:19913. DOI: 10.1038/s41598-019-53418-5. PMID: 31728010. PMCID: PMC6856386.
Article
34. Gao L, Li Y, Yang YJ, Zhang DY. 2021; The effect of moderate-intensity treadmill exercise on bone mass and the transcription of peripheral blood mononuclear cells in ovariectomized rats. Front Physiol. 12:729910. DOI: 10.3389/fphys.2021.729910. PMID: 34777002. PMCID: PMC8589120.
Article
35. Wu Y, Liu X, Han Y, Li L, Jian M, Sun G, Nie J. 2022; Peripheral blood mononuclear cells regulate differentially expressed proteins in the proximal sciatic nerve of rats after transection anastomosis. Neuroscience. 491:146–55. DOI: 10.1016/j.neuroscience.2022.03.041. PMID: 35395357.
Article
36. Kang J, Hur J, Kang JA, Lee HS, Jung H, Choi JI, Lee H, Kim YS, Ahn Y, Kim HS. 2016; Priming mobilized peripheral blood mononuclear cells with the "activated platelet supernatant" enhances the efficacy of cell therapy for myocardial infarction of rats. Cardiovasc Ther. 34:245–53. DOI: 10.1111/1755-5922.12194. PMID: 27214098.
Article
37. Ben-Slama I, Mrad I, Rihane N, Mir LE, Sakly M, Amara S. 2015; Sub-acute oral toxicity of zinc oxide nanoparticles in male rats. J Nanomed Nanotechnol. 6:284. DOI: 10.4172/2157-7439.1000284.
Article
38. Alazzouni AS, Fathalla AS, Gabri MS, Dkhil MA, Hassan BN. 2020; Role of bone marrow derived-mesenchymal stem cells against gastric ulceration: histological, immunohistochemical and ultrastructural study. Saudi J Biol Sci. 27:3456–64. DOI: 10.1016/j.sjbs.2020.09.044. PMID: 33304156. PMCID: PMC7715057.
Article
39. Şerban GM, Mănescu IB, Manu DR, Dobreanu M. 2018; Optimization of a density gradient centrifugation protocol for isolation of peripheral blood mononuclear cells. Acta Med Marisiensis. 64:83–90. DOI: 10.2478/amma-2018-0011.
Article
40. Oellerich M, Dasgupta A. Personalized immunosuppression in transplantation: role of biomarker monitoring and therapeutic drug monitoring. Elsevier;2016. p. 200–26.
41. Escobar G, Escobar A, Ascui G, Tempio FI, Ortiz MC, Pérez CA, López MN. 2018; Pure platelet-rich plasma and supernatant of calcium-activated P-PRP induce different phenotypes of human macrophages. Regen Med. 13:427–41. DOI: 10.2217/rme-2017-0122. PMID: 29985755.
Article
42. Dhurat R, Sukesh M. 2014; Principles and methods of preparation of platelet-rich plasma: a review and author's perspective. J Cutan Aesthet Surg. 7:189–97. DOI: 10.4103/0974-2077.150734. PMID: 25722595. PMCID: PMC4338460.
Article
43. Jo CH, Roh YH, Kim JE, Shin S, Yoon KS. 2013; Optimizing platelet-rich plasma gel formation by varying time and gravitational forces during centrifugation. J Oral Implantol. 39:525–32. DOI: 10.1563/AAID-JOI-D-10-00155. PMID: 21480780.
Article
44. Cavallo C, Roffi A, Grigolo B, Mariani E, Pratelli L, Merli G, Kon E, Marcacci M, Filardo G. 2016; Platelet-rich plasma: the choice of activation method affects the release of bioactive molecules. Biomed Res Int. 2016:6591717. DOI: 10.1155/2016/6591717. PMID: 27672658. PMCID: PMC5031826.
Article
45. Gaertner DJ, Hallman TM, Hankenson FC, Batchelder MA. Fish RE, Brown MJ, Danneman PJ, Karas AZ, editors. Anesthesia and analgesia for laboratory rodents. Anesthesia and Analgesia in Laboratory Animals. 2nd ed. Academic press;2008. p. 239–97. DOI: 10.1016/B978-012373898-1.50014-0.
Article
46. Bancroft JD, Gamble M. Theory and practice of histological techniques. 6th ed. Elsevier;2008. p. 126–7.
47. Ramos-Vara JA, Kiupel M, Baszler T, Bliven L, Brodersen B, Chelack B, Czub S, Del Piero F, Dial S, Ehrhart EJ, Graham T, Manning L, Paulsen D, Valli VE, West K. 2008; Suggested guidelines for immunohistochemical techniques in veterinary diagnostic laboratories. J Vet Diagn Invest. 20:393–413. DOI: 10.1177/104063870802000401. PMID: 18599844.
Article
48. Kim MR, Kim TI, Choi BR, Kim MB, Cho IJ, Lee KW, Ku SK. 2021; Brassica oleracea prevents HCl/ethanol-induced gastric damages in mice. Appl Sci. 11:16. DOI: 10.3390/app11010016.
49. Dawson BK, Trapp RG. Basic and clinical biostatistics. 3rd ed. Mcgraw-Hill;2000. p. 161–218.
50. Aboulhoda BE, Abdeltawab DA, Rashed LA, Abd Alla MF, Yassa HD. 2020; Hepatotoxic effect of oral zinc oxide nanoparticles and the ameliorating role of selenium in rats: a histological, immunohistochemical and molecular study. Tissue Cell. 67:101441. DOI: 10.1016/j.tice.2020.101441. PMID: 32949962.
Article
51. Elshama SS, El-Kenawy AEM, Osman HEH. 2017; Histopathological study of zinc oxide nanoparticle-induced neurotoxicity in rats. Toxicology. 13:95–103.
52. Jeong SH, Kim HJ, Ryu HJ, Ryu WI, Park YH, Bae HC, Jang YS, Son SW. 2013; ZnO nanoparticles induce TNF-α expression via ROS-ERK-Egr-1 pathway in human keratinocytes. J Dermatol Sci. 72:263–73. DOI: 10.1016/j.jdermsci.2013.08.002. PMID: 24001789.
Article
53. Elshakaa N, Bahaa N, Zeid AA, Latif HA. 2021; A histological and immunohistochemical study on the effect of zinc oxide nanoparticles on rat lung tissue. QJM. 114 Suppl 1:hcab099.007. DOI: 10.1093/qjmed/hcab099.007.
Article
54. Xiong P, Huang X, Ye N, Lu Q, Zhang G, Peng S, Wang H, Liu Y. 2022; Cytotoxicity of metal-based nanoparticles: from mechanisms and methods of evaluation to pathological manifestations. Adv Sci (Weinh). 9:e2106049. DOI: 10.1002/advs.202106049. PMID: 35343105. PMCID: PMC9165481.
Article
55. Liang X, Zhang D, Liu W, Yan Y, Zhou F, Wu W, Yan Z. 2017; Reactive oxygen species trigger NF-κB-mediated NLRP3 inflammasome activation induced by zinc oxide nanoparticles in A549 cells. Toxicol Ind Health. 33:737–45. DOI: 10.1177/0748233717712409. PMID: 28870124.
Article
56. Lim JW, Kim H, Kim KH. 2001; Nuclear factor-kappaB regulates cyclooxygenase-2 expression and cell proliferation in human gastric cancer cells. Lab Invest. 81:349–60. DOI: 10.1038/labinvest.3780243. PMID: 11310828.
57. Kim DY, Kim JH, Lee JC, Won MH, Yang SR, Kim HC, Wie MB. 2019; Zinc oxide nanoparticles exhibit both cyclooxygenase- and lipoxygenase-mediated apoptosis in human bone marrow-derived mesenchymal stem cells. Toxicol Res. 35:83–91. DOI: 10.5487/TR.2019.35.1.083. PMID: 30766660. PMCID: PMC6354944.
Article
58. Song WJ, Jeong MS, Choi DM, Kim KN, Wie MB. 2019; Zinc oxide nanoparticles induce autophagy and apoptosis via oxidative injury and pro-inflammatory cytokines in primary astrocyte cultures. Nanomaterials (Basel). 9:1043. DOI: 10.3390/nano9071043. PMID: 31330912. PMCID: PMC6669602.
Article
59. Patrón-Romero L, Luque-Morales PA, Loera-Castañeda V, Lares-Asseff I, Leal-Ávila MÁ, Alvelais-Palacios JA, Plasencia-López I, Almanza-Reyes H. 2022; Mitochondrial dysfunction induced by zinc oxide nanoparticles. Crystals. 12:1089. DOI: 10.3390/cryst12081089.
Article
60. Nassar SA, Ghonemy OI, Awwad MH, Mahmoud MSM, Alsagati YMB. 2017; Cyto and genotoxic effects of zinc oxide nanoparticles on testicular tissue of albino rat and the protective role of vitamin E. Transylv Rev. 25:5809–19.
61. Srivastav AK, Kumar A, Prakash J, Singh D, Jagdale P, Shankar J, Kumar M. 2017; Genotoxicity evaluation of zinc oxide nanoparticles in Swiss mice after oral administration using chromosomal aberration, micronuclei, semen analysis, and RAPD profile. Toxicol Ind Health. 33:821–34. DOI: 10.1177/0748233717717842. PMID: 28950792.
Article
62. Almansour M, Alarifi S, Melhim W, Jarrar BM. 2019; Nephron ultrastructural alterations induced by zinc oxide nanoparticles: an electron microscopic study. IET Nanobiotechnol. 13:515–21. DOI: 10.1049/iet-nbt.2018.5219. PMCID: PMC8676027.
Article
63. Müller KH, Kulkarni J, Motskin M, Goode A, Winship P, Skepper JN, Ryan MP, Porter AE. 2010; pH-dependent toxicity of high aspect ratio ZnO nanowires in macrophages due to intracellular dissolution. ACS Nano. 4:6767–79. DOI: 10.1021/nn101192z. PMID: 20949917.
Article
64. Hamza SA, Aly HM, Soliman SO, Abdallah DM. 2016; Ultrastructural study of the effect of zinc oxide nanoparticles on rat parotid salivary glands and the protective role of quercetin. Alex Dent J. 41:232–7. DOI: 10.21608/adjalexu.2016.58053.
Article
65. Kao YY, Chen YC, Cheng TJ, Chiung YM, Liu PS. 2012; Zinc oxide nanoparticles interfere with zinc ion homeostasis to cause cytotoxicity. Toxicol Sci. 125:462–72. DOI: 10.1093/toxsci/kfr319. PMID: 22112499.
Article
66. Ornellas FM, Ornellas DS, Martini SV, Castiglione RC, Ventura GM, Rocco PR, Gutfilen B, de Souza SA, Takiya CM, Morales MM. 2017; Bone marrow-derived mononuclear cell therapy accelerates renal ischemia-reperfusion injury recovery by modulating inflammatory, antioxidant and apoptotic related molecules. Cell Physiol Biochem. 41:1736–52. DOI: 10.1159/000471866. PMID: 28365681.
Article
67. Ramli Y, Alwahdy AS, Kurniawan M, Juliandi B, Wuyung PE, Susanto YDB. 2017; Intravenous versus intraarterial transplantation of human umbilical cord blood mononuclear cells for brain ischemia in rats. Hayati. 24:187–94. DOI: 10.1016/j.hjb.2017.11.002.
Article
68. Huang Q, Liu B, Jiang R, Liao S, Wei Z, Bi Y, Liu X, Deng R, Jin Y, Tan Y, Yang Y, Qin A. 2019; G-CSF-mobilized peripheral blood mononuclear cells combined with platelet-rich plasma accelerate restoration of ovarian function in cyclophosphamide-induced POI rats. Biol Reprod. 101:91–101. Erratum in: Biol Reprod 2020;102:1145. DOI: 10.1093/biolre/ioz077. PMID: 31034039.
Article
69. Pyšná A, Bém R, Němcová A, Fejfarová V, Jirkovská A, Hazdrová J, Jude EB, Dubský M. 2019; Endothelial progenitor cells biology in diabetes mellitus and peripheral arterial disease and their therapeutic potential. Stem Cell Rev Rep. 15:157–65. DOI: 10.1007/s12015-018-9863-4. PMID: 30413930.
Article
70. Zhang M, Huang B. 2012; The multi-differentiation potential of peripheral blood mononuclear cells. Stem Cell Res Ther. 3:48. DOI: 10.1186/scrt139. PMID: 23200034. PMCID: PMC3580478.
Article
71. Nie Z, Xu L, Li C, Tian T, Xie P, Chen X, Li B. 2016; Association of endothelial progenitor cells and peptic ulcer treatment in patients with type 2 diabetes mellitus. Exp Ther Med. 11:1581–6. DOI: 10.3892/etm.2016.3114. PMID: 27168776. PMCID: PMC4840543.
Article
72. Panahipour L, Kochergina E, Laggner M, Zimmermann M, Mildner M, Ankersmit HJ, Gruber R. 2020; Role for lipids secreted by irradiated peripheral blood mononuclear cells in inflammatory resolution in vitro. Int J Mol Sci. 21:4694. DOI: 10.3390/ijms21134694. PMID: 32630157. PMCID: PMC7370068.
Article
73. Beer L, Zimmermann M, Mitterbauer A, Ellinger A, Gruber F, Narzt MS, Zellner M, Gyöngyösi M, Madlener S, Simader E, Gabriel C, Mildner M, Ankersmit HJ. 2015; Analysis of the secretome of apoptotic peripheral blood mononuclear cells: impact of released proteins and exosomes for tissue regeneration. Sci Rep. 5:16662. DOI: 10.1038/srep16662. PMID: 26567861. PMCID: PMC4645175.
Article
74. Mildner CS, Copic D, Zimmermann M, Lichtenauer M, Direder M, Klas K, Bormann D, Gugerell A, Moser B, Hoetzenecker K, Beer L, Gyöngyösi M, Ankersmit HJ, Laggner M. 2022; Secretome of stressed peripheral blood mononuclear cells alters transcriptome signature in heart, liver, and spleen after an experimental acute myocardial infarction: an in silico analysis. Biology (Basel). 11:116. DOI: 10.3390/biology11010116. PMID: 35053121. PMCID: PMC8772778.
Article
75. Lichtenauer M, Mildner M, Hoetzenecker K, Zimmermann M, Podesser BK, Sipos W, Berényi E, Dworschak M, Tschachler E, Gyöngyösi M, Ankersmit HJ. 2011; Secretome of apoptotic peripheral blood cells (APOSEC) confers cytoprotection to cardiomyocytes and inhibits tissue remodelling after acute myocardial infarction: a preclinical study. Basic Res Cardiol. 106:1283–97. DOI: 10.1007/s00395-011-0224-6. PMID: 21952733. PMCID: PMC3228946.
Article
76. Gudbrandsdottir S, Hasselbalch HC, Nielsen CH. 2013; Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes. J Immunol. 191:4059–67. DOI: 10.4049/jimmunol.1201103. PMID: 24048901.
Article
77. Qian Y, Han Q, Chen W, Song J, Zhao X, Ouyang Y, Yuan W, Fan C. 2017; Platelet-rich plasma derived growth factors contribute to stem cell differentiation in musculoskeletal regeneration. Front Chem. 5:89. DOI: 10.3389/fchem.2017.00089. PMID: 29164105. PMCID: PMC5671651.
Article
78. Ahn JY, Hong YH, Kim KC, Kim JH, Lee SY, Lee JR, Lee EJ. 2022; Effect of human peripheral blood mononuclear cells on mouse endometrial cell proliferation: a potential therapeutics for endometrial regeneration. Gynecol Obstet Invest. 87:105–15. DOI: 10.1159/000524232. PMID: 35350012.
Article
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