Interface interaction between high-siliceous/calcareous mineral granules and model cell membranes dominated by electrostatic force

Abstract

High-siliceous/calcareous mineral granules may cause cytotoxicity by attaching to cell membranes. In this research, giant (GUVs) and small unilamellar vesicles (SUVs) were used as model membranes for studying the interaction between high-siliceous/calcareous mineral granules (micro calcite, micro quartz, nano calcium carbonate, and nano silica) and artificial membranes. Confocal laser scanning microscopy (CLSM) and fluorescence labeling experiments suggest that nano calcium carbonate (nano CaCO3) and nano silica (nano SiO2) induce gelation by disrupting the oppositely charged membranes, indicating the important role of electrostatic forces. Thereby, the mineral granule size affects the electrostatic interactions and thus leading to the damage of the membranes. FTIR spectra and molecular dynamics reveal that mineral granules mainly interact with -PO2, -OH, and -C-N(CH3)3+ groups in phospholipids. The electrostatic force between nano minerals and phospholipids is greater in the case SiO2 when compared to CaCO3. Moreover, nano SiO2 forms the strongest hydrogen bond with the -PO2 group as confirmed by FTIR. Thus, nano SiO2 causes the greatest damage to membranes. This research provides a deeper understanding of the mechanism regarding the interaction between inhalable mineral granules and cell membranes.

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References

  1. Akashi K, Miyata H, Itoh H, Kinosita K (1996) Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. Prog Biophys Mol Biol 71(6):3242–3250

    CAS  Google Scholar 

  2. Arrondo JLR, Goñi FM, Macarulla JM (1984) Infrared spectroscopy of phosphatidylcholines in aqueous suspension–A study of the phosphate group vibrations. BBA-Lipid Lipid Met 794(1):165–168

    CAS  Article  Google Scholar 

  3. Awadh SM (2012) Geochemistry and mineralogical composition of the airborne particles of sand dunes and dust storms settled in Iraq and their environmental impacts. Environ Earth Sci 66:2247–2256

    CAS  Article  Google Scholar 

  4. Bihan OL, Bonnafous P, Marak L, Bickel T, Trépout S, Mornet S, Haas FD, Talbot H, Taveau JC, Lambert O (2009) Cryo-electron tomography of nanoparticle transmigration into liposome. J Struct Biol 168(3):419–425

    Article  CAS  Google Scholar 

  5. Binder H, ZschöRnig O (2002) The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes. Chem Phys Lipids 115(1-2):39–61

    CAS  Article  Google Scholar 

  6. Chang M, Yun HL, Dong SS, Zhang LY, Zhen MM, Jiao YY, Yu HW (2016) Infrared spectroscopy study of sodium bicarbonate. Infrared Technol 38(09):803–810

    Google Scholar 

  7. Chen Y, Xie SD (2014) Characteristics and formation mechanism of a heavy air pollution episode caused by biomass burning in Chengdu, Southwest China. Sci Total Environ 473-474:507–517

    CAS  Article  Google Scholar 

  8. Chen YJ, Shi ZB, He KB, Ma YL, Liu Y (2007) Physico-chemical characteristics of individual mineral particles collected during dust storm periods in beijing. Res Environ Sci 20(1):52–57

    CAS  Google Scholar 

  9. Cho NJ, Frank CW, Kasemo B, Höök F (2010) Quartz crystal microbalance with dissipation monitoring of supported lipid bilayers on various substrates. Nat Protoc 5(6):1096–1106

    CAS  Article  Google Scholar 

  10. Cho EC, Zhang Q, Xia YN (2011) The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nat Nanotechnol 6(6):385–391

    CAS  Article  Google Scholar 

  11. Choimet M, Tourrette A, Marsan O, Rassu G, Drouet C (2020) Bio-inspired apatite particles limit skin penetration of drugs for dermatology applications. Acta Biomater 111:418–428

    CAS  Article  Google Scholar 

  12. Contado C, Mejia J, García OL, Piret JP, Dumortier E, Toussaint O, Lucas S (2016) Physicochemical and toxicological evaluation of silica nanoparticles suitable for food and consumer products collected by following the EC recommendation. Anal Bioanal Chem 408(1):271–286

    CAS  Article  Google Scholar 

  13. Dai QW, Han LB, Deng JJ, Zhao YL, Dang Z, Tan DY, Dong FQ (2018) The interface interaction behavior between E. coli and two kinds of fibrous minerals. Environ Sci Pollut Res 25(23):22420–22428

    CAS  Article  Google Scholar 

  14. Deng X, Zhang F, Wang L, Rui W, Long F, Zhao Y, Chen DL, Ding WJ (2014) Airborne fine particulate matter induces multiple cell death pathways in human lung epithelial cells. Apoptosis 19(7):1099–1112

    CAS  Article  Google Scholar 

  15. Ding WJ, An YG, Yang L, Liao ZJ, Zhang XY, Jiang K (2005) Study on IR of interaction of three modified-starchs and crystallization of calcium carbonate. Spectrosc Spectr Anal 25(5):701–704

    CAS  Google Scholar 

  16. Dong FQ, He XC, Li GW (2005) Study on the basic characteristics of several atmospheric dusts in the northern China. J Mineral Petrol 25(3):114–117

    Google Scholar 

  17. Dong FQ, Guo YT, Liu MX, Zhou L, Zhou Q, Li HL (2018) Spectroscopic evidence and molecular simulation investigation of the bonding interaction between lysine and montmorillonite: Implications for the distribution of soil organic nitrogen. Appl Clay Sci 159:3–9

    CAS  Article  Google Scholar 

  18. Gao YR, Jia YQ, Zhao YD, Wang CX, Zheng BB, Yang FY (2014) Effects of nano-silica and micro-silica particles on cytotoxicity and secretion of inflammatory factors in A549 cells. J Environ Hygiene 6:518–522

    Google Scholar 

  19. Gaus K, Gratton E, Kable E, Jones AS (2003) Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc Natl Acad Sci 100(26):15554–15559

    CAS  Article  Google Scholar 

  20. Guo YT (2016) Interaction of high-silicon-calcium ultrafine mineral granules with cell wall/membrane structural molecules of human body common bacteria. Dissertation, Southwest University of Science and Technology.

  21. Huebert BJ, Wang MX, Lu WX (2017) Atmospheric nitrate, sulfate, ammonium and calcium concentrations in China. Tellus Ser B Chem Phys Meteorol 40:260–269

    Article  Google Scholar 

  22. Huo TT, Dong FQ, Deng JJ, Zhang QB, He XC, Sun DP (2016) Comparation of toxic effect of silicious mineral dusts on lung epithelial A549 cells. Environ Sci 37(11):4410–4418

    Google Scholar 

  23. Jan R, Roy R, Bhor R, Pai K, Satsangi PG (2020) Toxicological screening of airborne particulate matter in atmosphere of Pune: reactive oxygen species and cellular toxicity. Environ Pollut 261:113724

    CAS  Article  Google Scholar 

  24. Jiang W, Yang K, Vachet RW, Xing BS (2010) Interaction between oxide nanoparticles and biomolecules of the bacterial cell envelope as examined by infrared spectroscopy. Langmuir 26(23):18071–18077

    CAS  Article  Google Scholar 

  25. Jiang W, Ghosh S, Song L, Vachet RW, Xing BS (2013) Effect of Al2O3 nanoparticles on bacterial membrane amphiphilic biomolecules. Colloid Surf B 102:292–299

    CAS  Article  Google Scholar 

  26. Jiang Q, Sun YL, Wang Z, Yin Y (2015) Aerosol composition and sources during the Chinese Spring Festival: fireworks, secondary aerosol, and holiday effects. Atmos Chem Phys 15(11):20617–20646

    Article  CAS  Google Scholar 

  27. Kaufhold S, Hein M, Dohrmann R, Ufer K (2012) Quantification of the mineralogical composition of clays using FTIR spectroscopy. Vib Spectrosc 59(3):29–39

    CAS  Article  Google Scholar 

  28. Kim KH, Kabir E, Kabir S (2015) A review on the human health impact of airborne particulate matter. Environ Int 74:136–143

    CAS  Article  Google Scholar 

  29. Kim JH, Son JW, Kim J, Kim MG, Jeong SH, Park TJ, Son SW, Ryu HJ (2020) Particulate matter (PM)(2.5) affects keratinocytes via endoplasmic reticulum (ER) stress-mediated suppression of apoptosis. Mol Cell Toxicol 16(2):129–137

    CAS  Article  Google Scholar 

  30. Kreyling WG, Hirn S, Möller W, Schleh C, Wenk A, Celik G, Lipka J, Schäffler M, Haberl N, Johnston BD, Sperling RA, Schmid G, Simon U, Parak WJ, Semmler-Behnke M (2013) Air-blood barrier translocation of tracheally instilled gold nanoparticles inversely depends on particle size. ACS Nano 8(1):222–233

    Article  CAS  Google Scholar 

  31. Larkin PJ (2011) Infrared and Raman spectroscopy; principles and spectral interpretation. Elsevier

  32. Laurencin M, Georgelin T, Malezieux B, Siaugue B (2010) Interactions between giant unilamellar vesicles and charged core-shell magnetic nanoparticles. Langmuir 26(20):16025–16030

    CAS  Article  Google Scholar 

  33. Lewinski N, Colvin V, Drezek R (2008) Cytotoxicity of Nanoparticles. Small 4(1):26–49

    CAS  Article  Google Scholar 

  34. Lewis RNAH, McElhaney RN, Pohle W, Mantsch HH (1994) Components of the carbonyl stretching band in the infrared spectra of hydrated 1,2-diacylglycerolipid bilayers: a reevaluation. Biophys J 67(6):2367–2375

    CAS  Article  Google Scholar 

  35. Li ZY, Xu RK (2015) Study on effect of kaolinite colloids on zeta potential of Al oxide coated quartz with streaming potential method. Acta Pedol Sin 52(06):1301–1310

    Google Scholar 

  36. Li WJ, Shao LY, Shi ZB, Li JJ, Yang SS (2008) Physical and chemical characteristics of individual mineral particles in an urban fog episode. Environ Sci 29(1):253–258

    Google Scholar 

  37. Liang CH, Yeh LH, Liao PW, Chou TH (2015) Characterization and in vitro biocompatibility of catanionic assemblies formed with oppositely charged dicetyl amphiphiles. Colloid Surf B 126:10–17

    CAS  Article  Google Scholar 

  38. Liao ZH, Sun JR, Liu J, Guo S, Fan SJ (2018) Long-term trends in ambient particulate matter, chemical composition, and associated health risk and mortality burden in Hong Kong (1995–2016). Air Qual Atmos Health 11:773–783

    CAS  Article  Google Scholar 

  39. Lin YS, Haynes C (2010) Impacts of mesoporous silica nanoparticle size, pore ordering, and pore integrity on hemolytic activity. J Am Chem Soc 132(13):4834–4842

    CAS  Article  Google Scholar 

  40. Lozano O, Silva-Platas C, Chapoy-Villanueva H, Pérez BE, Lees JG, Ramachandra CJA, Contreras-Torres FF, Lázaro-Alfaro A, Luna-Figueroa E, Bernal-Ramírez J, Gordillo-Galeano A, Benitez A, Oropeza-Almazán Y, Castillo EC, Koh PL, Hausenloy DJ, Lim SY, García-Rivas G (2020) Amorphous SiO2 nanoparticles promote cardiac dysfunction via the opening of the mitochondrial permeability transition pore in rat heart and human cardiomyocytes. Part Fibre Toxicol 17(1):15

    CAS  Article  Google Scholar 

  41. Magnabosco G, Giosia MD, Polishchuk I, Weber E, Fermani S, Bottoni A, Zerbetto F, Pokroy B, Rapino S, Falini G, Calvaresi M (2016) Calcite single crystals as hosts for atomic-scale entrapment and slow release of drugs. Adv Healthc Mater 4(10):1510–1516

    Article  CAS  Google Scholar 

  42. Montis C, Baglioni P, Berti D (2013) Monitoring the interaction of nucleolipoplexes with model membranes. Soft Matter 10(1):39–43

    Article  Google Scholar 

  43. Najafi MS, Khoshakhllagh F, Zamanzadeh SM, Shirazi MH, Samadi M, Hajikhani S (2014) Characteristics of TSP loads during the middle east springtime dust storm (MESDS) in western Iran. Arab J Geosci 7(12):5367–5381

    CAS  Article  Google Scholar 

  44. Nishimori H, Kondoh M, Isoda K, Tsunoda SI, Tsutsumi Y, Yagi K (2009) Silica nanoparticles as hepatotoxicants. Eur J Pharm Biopharm 72(3):496–501

    CAS  Article  Google Scholar 

  45. Nowak S, Lafon S, Caquineau S, Journet E, Laurent B (2018) Quantitative study of the mineralogical composition of mineral dust aerosols by X-ray diffraction. Talanta 186:133–139

    CAS  Article  Google Scholar 

  46. Okada K, Qin Y, Kai K (2005) Elemental composition and mixing properties of atmospheric mineral particles collected in Hohhot, China. Atmos Res 73(1-2):45–67

    CAS  Article  Google Scholar 

  47. Orona NS, Astort F, Maglione GA, Saldiva PHN, Yakisich JS, Tasat DR (2014) Direct and indirect air particle cytotoxicity in human alveolar epithelial cells. Toxicol in Vitro 28(5):796–802

    CAS  Article  Google Scholar 

  48. Pang YT, Huang YJ, Luo XS, Chen Q, Zhao Z, Tang MW, Hong WY, Chen JS, Li HB (2020) In-vitro human lung cell injuries induced by urban PM2.5 during a severe air pollution episode: variations associated with particle components. Ecotox Environ Safe (206): 111406.

  49. Papadia K, Markoutsa E, Antimisiaris SG (2016) How do the physicochemical properties of nanoliposomes affect their interactions with the hCMEC/D3 cellular model of the BBB? Int J Pharm 509(1-2):431–438

    CAS  Article  Google Scholar 

  50. Rauf N, Tahir D, Arbiansyah M (2016) Structural analysis of bioceramic materials for denture application. Am Inst Phys Conf Ser 1719(1):030030

    Google Scholar 

  51. Roszak J, Catalán J, Järventaus H, Lindberg HK, Suhonen S, Vippola M, Stępnik M, Norppa H (2016) Effect of particle size and dispersion status on cytotoxicity and genotoxicity of zinc oxide in human bronchial epithelial cells. Mutat Res-Gen Tox En 805:7–18

    CAS  Article  Google Scholar 

  52. Rozalen M, Ramos ME, Huertas FJ, Fiore S, Gervilla F (2013) Dissolution kinetics and biodurability of tremolite particles in mimicked lung fluids: effect of citrate and oxalate. J Asian Earth Sci 77:318–326

    Article  Google Scholar 

  53. Santhosh PB, Velikonja A, Perutkova Š, Gongadze E, Kulkarni M, Genova J, Eleršič K, Iglič A, Kralj-Iglič V, Ulrih NP (2014) Influence of nanoparticle–membrane electrostatic interactions on membrane fluidity and bending elasticity. Chem Phys Lipids 178:52–62

    CAS  Article  Google Scholar 

  54. Sohal IS, Cho YK, O’Fallon KS, Gaines P, Demokritou P, Bello D (2018) Dissolution behavior and biodurability of ingested engineered nanomaterials in the gastrointestinal environment. ACS Nano 12(8):8115–8128

    CAS  Article  Google Scholar 

  55. Tao YJ, Zeng YL, Deng JJ, Dong FQ, Wang LM, Huo TY (2016) Study on genotoxicity of six main kinds of PM2.5 mineral particles in A549 cell. Industrial Health Occup Dis 5:321–325

    Google Scholar 

  56. Tarn D, Ashley CE, Xue M, Carnes EC (2013) Mesoporous silica nanoparticle nanocarriers: biofunctionality and biocompatibility. Acc Chem Res 46(3):792–801

    CAS  Article  Google Scholar 

  57. Vargas OAR, Serrano J, Rojas-Bracho L, Miranda J (2011) In vitro biological effects of airborne PM2.5 and PM10 from a semi-desert city on the Mexico-US border. Chemosphere 83(4):618–626

    Article  CAS  Google Scholar 

  58. Wang B, Zhang LF, Bae SC, Granick S (2008) Nanoparticle-induced surface reconstruction of phospholipid membranes. Proc Natl Acad Sci U S A 105(47):18171–18175

    CAS  Article  Google Scholar 

  59. Wang ZN, Wang XD, Ding WD, Wang MQ, Qi X, Gao CJ (2015) Impact of monoolein on aquaporin1-based supported lipid bilayer membranes. Sci Technol Adv Mater 16(4):045005

    Article  CAS  Google Scholar 

  60. Wang Z, Dong SP, Liang HD, Chen Y, Zhan Q (2018) Study on environmental individual particles in Wuda-Wusitai Industrial Park, Inner Mongolia. China Environ Sci 38(2):478–489

    Google Scholar 

  61. Wang F, Wang J, Han MM, Jia CQ, Zhou YY (2019) Heavy metal characteristics and health risk assessment of PM2.5 in students dormitories in a university in Nanjing, China. Build Environ 160:106206

    Article  Google Scholar 

  62. Wang JJ, Huang Y, Li T, He M, Cheng X, Su T, Ni SJ, Zhang CJ (2020a) Contamination, morphological status and sources of atmospheric dust in different land-using areas of a steel-industry city, China. Atmos Pollut Res 11(2):283–289

    CAS  Article  Google Scholar 

  63. Wang XG, Sun TS, Zhu H, Han T, Wang J, Dai HL (2020b) Roles of pH, cation valence, and ionic strength in the stability and aggregation behavior of zinc oxide nanoparticles. J Environ Manag 267:110656

    CAS  Article  Google Scholar 

  64. Wei XR, Qu XL, Ding L, Hu JT, Jiang W (2016) Role of bovine serum albumin and humic acid in the interaction between SiO2 nanoparticles and model cell membranes. Environ Pollut 219:1–8

    CAS  Article  Google Scholar 

  65. Wei XR, Yu JC, Ding L, Hu JT, Jiang W (2017) Effect of oxide nanoparticles on the morphology and fluidity of phospholipid membranes and the role of hydrogen bonds. J Environ Sci 57:221–230

    CAS  Article  Google Scholar 

  66. Wong PTT, Papavassiliou ED, Rigas B (1991) Phosphodiester stretching bands in the infrared spectra of human tissues and cultured cells. Appl Spectrosc 45(9):1563–1567

    CAS  Article  Google Scholar 

  67. Xiao YT, Lasaga AC (1994) Ab initio quantum mechanical studies of the kinetics and mechanisms of silicate dissolution: H+(H3O+) catalysis. Geochim Cosmochim Acta 58(24):5379–5400

    CAS  Article  Google Scholar 

  68. Xiao YT, Lasaga AC (1996) Ab initio quantum mechanical studies of the kinetics and mechanisms of quartz dissolution: OH- catalysis. Geochim Cosmochim Acta 60(13):2283–2295

    CAS  Article  Google Scholar 

  69. Xu LZ, Tian M (2020) Respiratory exposure to PM2.5 soluble extract disrupts mucosal barrier function and promotes the development of experimental asthma. Sci Total Environ 730:139145

    Article  CAS  Google Scholar 

  70. Yang YY, Liu LY, Xiong YY, Zhang GM, Wen HM, Lei J, Guo LL, Lyu YL (2016) A comparative study on physicochemical characteristics of household dust from a metropolitan city and a remote village in China. Atmos Pollut Res 7(6):1090–1100

    Article  Google Scholar 

  71. Yu Y, Anthony SM, Zhang LF, Bae SC, Granick S (2014) Cationic nanoparticles stabilize zwitterionic liposomes better than anionic ones. J Phys Chem C 111(23):3692–3700

    Google Scholar 

  72. Yuan CB, Zhao DQ, Liu AZ, Ni JZ (1995) A NMR study of the interaction of silica with dipalmitoylphosphatidylcholine liposomes. J Colloid Interface Sci 172(2):536–538

    Article  Google Scholar 

  73. Yuan PQ, Kong N, Cheng ZM, Semiat R (2009) Electrostatic potential on anti-scalants modified CaCO3 (104) surface: a molecular simulation study. Desalination 238(1-3):246–256

    CAS  Article  Google Scholar 

  74. Zhang XL, Wu GJ, Yue YH, Zhang CL (2011) Mineral composition and morphology of individual dust fall particulates over Lhasa in summer. Acta Petrol Et Min 30(1):127–134

    CAS  Google Scholar 

  75. Zhao YL (2018a) The interfacial interaction and mechanisms of the micro-nano mineral dust/common bacteria complex. Dissertation, Southwest University of Science and Technology

  76. Zhao SR (2018b) Molecular dynamics study on the interaction of carbon nanotubes and phospholipid bilayers. Dissertation, Harbin Institute of Technology

  77. Zhou CH, Keeling J (2013) Fundamental and applied research on clay minerals: From climate and environment to nanotechnology. Appl Clay Sci 74:3–9

    CAS  Article  Google Scholar 

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Acknowledgements

The authors thank professor Riehle Frank for language help.

Funding

This work was supported by the National Natural Science Foundation of China (Grant Number: 41831285 and 41802037), National Basic Research Program of China (973 Program: 2014CB846003), National Key R&D Program of China (2016YFC0502204), Longshan Academic Talent Research Supporting Program of SWUST (18LZX507), and the Postgraduate Innovation Fund Project by Southwest University of Science and Technology (19ycx0076).

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All authors contributed to this manuscript. Faqin Dong, Mingxue Liu, and Mulan Chen conceived and designed the study. Mulan Chen and Shi Ou performed the experiments. Mulan Chen, Hailong Li, and Wei Zhang performed the data analysis. Mulan Chen wrote this manuscript. Faqin Dong, Mingxue Liu, and Yulian Zhao guided the structure and contents of the paper, and improved earlier drafts.

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Chen, M., Dong, F., Li, H. et al. Interface interaction between high-siliceous/calcareous mineral granules and model cell membranes dominated by electrostatic force. Environ Sci Pollut Res (2021). https://doi.org/10.1007/s11356-021-12584-8

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Keywords

  • Nano CaCO3
  • Nano SiO2
  • Membrane integrity
  • Membrane phase
  • Interface interaction
  • Molecular dynamics