Skip to main content

Implications of Biomolecular Corona for Molecular Imaging

Molecular Imaging and Biology volume 23, pages 1–10 (2021)Cite this article

Abstract

The development of nanoparticle probes has opened up new possibilities for molecular imaging in the era of precision medicine. There are a wide range of nanoprobes that are being used for various modalities that have demonstrated promising potential in early detection, disease monitoring, and theranostics. However, the rate of successful clinical translation of the nanoprobes is very low and is affected by the lack of our understanding about nanoparticle interaction with biological fluids after systemic administration, thus representing an unmet clinical need. One of the poorly understood issues relates to the formation of biomolecular corona, a layer of biomolecules formed on the surface of nanoscale materials during their interactions with biological fluids. The biomolecular corona has several significant effects on the biodistribution of nanoprobes and their imaging ability by (i) reducing their targeting efficacy and (ii) affecting the intrinsic imaging properties (e.g., contrast capacity of magnetic nanoprobes). This review provides insights on the importance of considering biomolecular corona in the development of nanoprobes, which may enable their more efficient utilization for molecular imaging applications.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Lee J-H, Huh Y-M, Jun Y-w et al (2007) Artificially engineered magnetic nanoparticles for ultra-sensitive molecular imaging. Nat Med 13:95–99

    CAS  PubMed  Google Scholar 

  2. Caracciolo G, Vali H, Moore A, Mahmoudi M (2019) Challenges in molecular diagnostic research in cancer nanotechnology. Nano Today 27:6–10

    Google Scholar 

  3. Xing H, Bu W, Zhang S, Zheng X, Li M, Chen F, He Q, Zhou L, Peng W, Hua Y, Shi J (2012) Multifunctional nanoprobes for upconversion fluorescence, MR and CT trimodal imaging. Biomaterials 33:1079–1089

    CAS  PubMed  Google Scholar 

  4. Whiting GT, Nikolopoulos N, Nikolopoulos I, Chowdhury AD, Weckhuysen BM (2019) Visualizing pore architecture and molecular transport boundaries in catalyst bodies with fluorescent nanoprobes. Nat Chem 11:23–31

    CAS  PubMed  Google Scholar 

  5. Pal S, Ray A, Andreou C et al (2019) DNA-enabled rational design of fluorescence-Raman bimodal nanoprobes for cancer imaging and therapy. Nat Commun 10:1–13

    CAS  Google Scholar 

  6. Wang S, Liu L, Fan Y, el-Toni AM, Alhoshan MS, Li D, Zhang F (2019) In vivo high-resolution ratiometric fluorescence imaging of inflammation using NIR-II nanoprobes with 1550 nm emission. Nano Let 19:2418–2427

    CAS  Google Scholar 

  7. Xu G, Qian Y, Zheng H, Qiao S, Yan D, Lu L, Wu L, Yang X, Luo Q, Zhang Z (2019) Long-distance tracing of the lymphatic system with a computed tomography/fluorescence dual-modality nanoprobe for surveying tumor lymphatic metastasis. Bioconjug Chem 30:1199–1209

    CAS  PubMed  Google Scholar 

  8. Mancebo DG, Becerro AI, Corral A et al (2020) Design of a nanoprobe for high field magnetic resonance imaging, dual energy X-ray computed tomography and luminescent imaging. J Colloid Interface Sci 573:278–286

    Google Scholar 

  9. Zeng S, Tsang M-K, Chan C-F, Wong K-L, Hao J (2012) PEG modified BaGdF5: Yb/Er nanoprobes for multi-modal upconversion fluorescent, in vivo X-ray computed tomography and biomagnetic imaging. Biomaterials 33:9232–9238

    CAS  PubMed  Google Scholar 

  10. Wang Y, Sun Z, Chen Z, Wu Y, Gu Y, Lin S, Wang Y (2019) In vivo photoacoustic/single-photon emission computed tomography imaging for dynamic monitoring of aggregation-enhanced photothermal nanoagents. Anal Chem 91:2128–2134

    CAS  PubMed  Google Scholar 

  11. Yang Y, Zhang L, Cai J, Li X, Cheng D, Su H, Zhang J, Liu S, Shi H, Zhang Y, Zhang C (2016) Tumor angiogenesis targeted radiosensitization therapy using gold nanoprobes guided by MRI/SPECT imaging. ACS Appl Mater Interfaces 8:1718–1732

    CAS  PubMed  Google Scholar 

  12. Jing B, Qian R, Gai Y, Lan X, An R (2019) Multimodality PET/CT and NIRF imaging for image-guided surgery of colon cancer with exosomes based nanoprobe. J Nucl Med 60:662–662

    Google Scholar 

  13. Lahooti A, Shanehsazzadeh S, Laurent S (2019) Preliminary studies of 68Ga-NODA-USPION-BBN as a dual-modality contrast agent for use in positron emission tomography/magnetic resonance imaging. Nanotechnology 31:015102

    PubMed  Google Scholar 

  14. Zhan Y, Ai F, Chen F, Valdovinos HF, Orbay H, Sun H, Liang J, Barnhart TE, Tian J, Cai W (2016) Intrinsically zirconium-89 labeled Gd2O2S: Eu nanoprobes for in vivo positron emission tomography and gamma-ray-induced radioluminescence imaging. Small 12:2872–2876

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Park YI, Kim JH, Lee KT, Jeon KS, Na HB, Yu JH, Kim HM, Lee N, Choi SH, Baik SI, Kim H, Park SP, Park BJ, Kim YW, Lee SH, Yoon SY, Song IC, Moon WK, Suh YD, Hyeon T (2009) Nonblinking and nonbleaching upconverting nanoparticles as an optical imaging nanoprobe and T1 magnetic resonance imaging contrast agent. Adv Mater 21:4467–4471

    CAS  Google Scholar 

  16. Sharifi S, Seyednejad H, Laurent S, Atyabi F, Saei AA, Mahmoudi M (2015) Superparamagnetic iron oxide nanoparticles for in vivo molecular and cellular imaging. Contrast Media Mol Imaging 10:329–355

    CAS  PubMed  Google Scholar 

  17. Chen H, Song M, Tang J, Hu G, Xu S, Guo Z, Li N, Cui J, Zhang X, Chen X, Wang L (2016) Ultrahigh 19F loaded Cu1. 75S nanoprobes for simultaneous 19F magnetic resonance imaging and photothermal therapy. ACS Nano 10:1355–1362

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Yigit MV, Zhu L, Ifediba MA, Zhang Y, Carr K, Moore A, Medarova Z (2011) Noninvasive MRI-SERS imaging in living mice using an innately bimodal nanomaterial. ACS Nano 5:1056–1066

    CAS  PubMed  Google Scholar 

  19. Wang P, Yoo B, Yang J, Zhang X, Ross A, Pantazopoulos P, Dai G, Moore A (2014) GLP-1R–targeting magnetic nanoparticles for pancreatic islet imaging. Diabetes 63:1465–1474

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Huang X, Song J, Yung BC, Huang X, Xiong Y, Chen X (2018) Ratiometric optical nanoprobes enable accurate molecular detection and imaging. Chem Soc Rev 47:2873–2920

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Won J, Kim M, Yi Y-W, Kim YH, Jung N, Kim TK (2005) A magnetic nanoprobe technology for detecting molecular interactions in live cells. Science 309:121–125

    CAS  PubMed  Google Scholar 

  22. Zhu C, Zeng Z, Li H, Li F, Fan C, Zhang H (2013) Single-layer MoS2-based nanoprobes for homogeneous detection of biomolecules. J Am Chem Soc 135:5998–6001

    CAS  PubMed  Google Scholar 

  23. Wabuyele MB, Vo-Dinh T (2005) Detection of human immunodeficiency virus type 1 DNA sequence using plasmonics nanoprobes. Anal Chem 77:7810–7815

    CAS  PubMed  Google Scholar 

  24. Song S, Qin Y, He Y, Huang Q, Fan C, Chen H-Y (2010) Functional nanoprobes for ultrasensitive detection of biomolecules. Chem Soc Rev 39:4234–4243

    CAS  PubMed  Google Scholar 

  25. Walczyk D, Bombelli FB, Monopoli MP, Lynch I, Dawson KA (2010) What the cell “sees” in bionanoscience. J Am Chem Soc 132:5761–5768

    CAS  PubMed  Google Scholar 

  26. Monopoli MP, Åberg C, Salvati A, Dawson KA (2012) Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotech 7:779–786

    CAS  Google Scholar 

  27. Kelly PM, Åberg C, Polo E et al (2015) Mapping protein binding sites on the biomolecular corona of nanoparticles. Nat Nanotech 10:472

    CAS  Google Scholar 

  28. Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA (2008) Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc Natl Acad Sci U S A 105:14265–14270

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Mahmoudi M, Abdelmonem AM, Behzadi S, Clement JH, Dutz S, Ejtehadi MR, Hartmann R, Kantner K, Linne U, Maffre P, Metzler S, Moghadam MK, Pfeiffer C, Rezaei M, Ruiz-Lozano P, Serpooshan V, Shokrgozar MA, Nienhaus GU, Parak WJ (2013) Temperature: the “ignored” factor at the nanobio interface. ACS Nano 7:6555–6562

    CAS  PubMed  Google Scholar 

  30. Mirshafiee V, Kim R, Mahmoudi M, Kraft ML (2016) The importance of selecting a proper biological milieu for protein corona analysis in vitro: human plasma versus human serum. Int J Biochem Cell Biol 75:188–195

    CAS  PubMed  Google Scholar 

  31. Müller LK, Simon J, Rosenauer C, Mailänder V, Morsbach S, Landfester K (2018) The transferability from animal models to humans: challenges regarding aggregation and protein corona formation of nanoparticles. Biomacromolecules 19:374–385

    PubMed  Google Scholar 

  32. Ghavami M, Saffar S, Abd Emamy B, Peirovi A, Shokrgozar MA, Serpooshan V, Mahmoudi M (2013) Plasma concentration gradient influences the protein corona decoration on nanoparticles. RSC Adv 3:1119–1126

    CAS  Google Scholar 

  33. Mahmoudi M, Lynch I, Ejtehadi MR, Monopoli MP, Bombelli FB, Laurent S (2011) Protein− nanoparticle interactions: opportunities and challenges. Chem Rev 111:5610–5637

    CAS  PubMed  Google Scholar 

  34. Ashkarran AA, Dararatana N, Crespy D, Caracciolo G, Mahmoudi M (2020) Mapping the heterogeneity of protein corona by ex vivo magnetic levitation. Nanoscale 12:2374–2383

    CAS  PubMed  Google Scholar 

  35. Ashkarran AA, Mahmoudi M (2020) Magnetic levitation systems for disease diagnostics. Trends Biotechnol in press

  36. Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Baldelli Bombelli F, Dawson KA (2011) Physical− chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 133:2525–2534

    CAS  PubMed  Google Scholar 

  37. Deng ZJ, Liang M, Monteiro M, Toth I, Minchin RF (2011) Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation. Nat Nanotechnol 6:39–44

    CAS  PubMed  Google Scholar 

  38. Giulimondi F, Digiacomo L, Pozzi D et al (2019) Interplay of protein corona and immune cells controls blood residency of liposomes. Nat Commun 10:1–11

    Google Scholar 

  39. Mahmoudi M (2018) Antibody orientation determines corona mistargeting capability. Nat Nanotechnol 13:775–776

    CAS  PubMed  Google Scholar 

  40. Behzadi S, Serpooshan V, Sakhtianchi R, Müller B, Landfester K, Crespy D, Mahmoudi M (2014) Protein corona change the drug release profile of nanocarriers: the “overlooked” factor at the nanobio interface. Colloids Surf B Biointerfaces 123:143–149

    CAS  PubMed  Google Scholar 

  41. Sharifi S, Caracciolo G, Mahmoudi M (2020) Biomolecular corona affects controlled release of drug payloads from nanocarriers. Trends Pharmacol Sci 41:641–652

    CAS  PubMed  Google Scholar 

  42. Mahmoudi M, Simchi A, Imani M, Shokrgozar MA, Milani AS, Häfeli UO, Stroeve P (2010) A new approach for the in vitro identification of the cytotoxicity of superparamagnetic iron oxide nanoparticles. Colloids Surf B Biointerfaces 75:300–309

    CAS  PubMed  Google Scholar 

  43. Lesniak A, Fenaroli F, Monopoli MP, Åberg C, Dawson KA, Salvati A (2012) Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6:5845–5857

    CAS  PubMed  Google Scholar 

  44. Lesniak A, Salvati A, Santos-Martinez MJ, Radomski MW, Dawson KA, Åberg C (2013) Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. J Am Chem Soc 135:1438–1444

    CAS  PubMed  Google Scholar 

  45. Dutta D, Sundaram SK, Teeguarden JG, Riley BJ, Fifield LS, Jacobs JM, Addleman SR, Kaysen GA, Moudgil BM, Weber TJ (2007) Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol Sci 100:303–315

    CAS  PubMed  Google Scholar 

  46. Zanganeh S, Hutter G, Spitler R, Lenkov O, Mahmoudi M, Shaw A, Pajarinen JS, Nejadnik H, Goodman S, Moseley M, Coussens LM, Daldrup-Link HE (2016) Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues. Nat Nanotechnol 11:986–994

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Dobrovolskaia MA, Aggarwal P, Hall JB, McNeil SE (2008) Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. Mol Pharm 5:487–495

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Derakhshankhah H, Hajipour MJ, Barzegari E, Lotfabadi A, Ferdousi M, Saboury AA, Ng EP, Raoufi M, Awala H, Mintova S, Dinarvand R, Mahmoudi M (2016) Zeolite nanoparticles inhibit Aβ–fibrinogen interaction and formation of a consequent abnormal structural clot. ACS Appl Mater Interfaces 8:30768–30779

    CAS  PubMed  Google Scholar 

  49. Reddy ST, Van Der Vlies AJ, Simeoni E et al (2007) Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat Biotechnol 25:1159–1164

    CAS  PubMed  Google Scholar 

  50. Rahman M, Mahmoudi M (2015) Disease specific protein corona. Proc. SPIE 9338, Colloidal Nanoparticles for Biomedical Applications X, 93380V. https://doi.org/10.1117/12.2079771

  51. Tirtaatmadja N, Mortimer G, Ng E-P, Ahmad HA, Mintova S, Serpooshan V, Minchin RF, Mahmoudi M (2015) Nanoparticles-induced inflammatory cytokines in human plasma concentration manner: an ignored factor at the nanobio-interface. J Iranian Chem Soc 12:317–323

    CAS  Google Scholar 

  52. Caracciolo G, Farokhzad OC, Mahmoudi M (2017) Biological identity of nanoparticles in vivo: clinical implications of the protein corona. Trends Biotechnol 35:257–264

    CAS  PubMed  Google Scholar 

  53. Sakulkhu U, Maurizi L, Mahmoudi M, Motazacker M, Vries M, Gramoun A, Ollivier Beuzelin MG, Vallée JP, Rezaee F, Hofmann H (2014) Ex situ evaluation of the composition of protein corona of intravenously injected superparamagnetic nanoparticles in rats. Nanoscale 6:11439–11450

    CAS  PubMed  Google Scholar 

  54. Hadjidemetriou M, Al-Ahmady Z, Mazza M, Collins RF, Dawson K, Kostarelos K (2015) In vivo biomolecule corona around blood-circulating, clinically used and antibody-targeted lipid bilayer nanoscale vesicles. ACS Nano 9:8142–8156

    CAS  PubMed  Google Scholar 

  55. Behzadi S, Serpooshan V, Tao W, Hamaly MA, Alkawareek MY, Dreaden EC, Brown D, Alkilany AM, Farokhzad OC, Mahmoudi M (2017) Cellular uptake of nanoparticles: journey inside the cell. Chem Soc Rev 46:4218–4244

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Laurent S, Mahmoudi M (2011) Superparamagnetic iron oxide nanoparticles: promises for diagnosis and treatment of cancer. Int J Mol Epidemiol Genet 2:367–390

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Mirshafiee V, Mahmoudi M, Lou K, Cheng J, Kraft ML (2013) Protein corona significantly reduces active targeting yield. Chem Comm 49:2557–2559

    CAS  PubMed  Google Scholar 

  58. Salvati A, Pitek AS, Monopoli MP, Prapainop K, Bombelli FB, Hristov DR, Kelly PM, Åberg C, Mahon E, Dawson KA (2013) Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat Nanotechnol 8:137–143

    CAS  PubMed  Google Scholar 

  59. Wilhelm S, Tavares AJ, Dai Q et al (2016) Analysis of nanoparticle delivery to tumours. Nat Rev Mat 1:1–12

    Google Scholar 

  60. Mahmoudi M (2018) Debugging nano–bio interfaces: systematic strategies to accelerate clinical translation of nanotechnologies. Trends Biotechnol 36:755–769

    CAS  PubMed  Google Scholar 

  61. Serpooshan V, Sheibani S, Pushparaj P, Wojcik M, Jang AY, Santoso MR, Jang JH, Huang H, Safavi-Sohi R, Haghjoo N, Nejadnik H, Aghaverdi H, Vali H, Kinsella JM, Presley J, Xu K, Yang PCM, Mahmoudi M (2018) Effect of cell sex on uptake of nanoparticles: the overlooked factor at the nanobio interface. ACS Nano 12:2253–2266

    CAS  PubMed  Google Scholar 

  62. Moyano DF, Saha K, Prakash G, Yan B, Kong H, Yazdani M, Rotello VM (2014) Fabrication of corona-free nanoparticles with tunable hydrophobicity. ACS Nano 8:6748–6755

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Tonigold M, Simon J, Estupiñán D, Kokkinopoulou M, Reinholz J, Kintzel U, Kaltbeitzel A, Renz P, Domogalla MP, Steinbrink K, Lieberwirth I, Crespy D, Landfester K, Mailänder V (2018) Pre-adsorption of antibodies enables targeting of nanocarriers despite a biomolecular corona. Nat Nanotechnol 13:862–869

    CAS  PubMed  Google Scholar 

  64. Amiri H, Bordonali L, Lascialfari A, Wan S, Monopoli MP, Lynch I, Laurent S, Mahmoudi M (2013) Protein corona affects the relaxivity and MRI contrast efficiency of magnetic nanoparticles. Nanoscale 5:8656–8665

    CAS  PubMed  Google Scholar 

  65. Guckeisen T, Hosseinpour S, Peukert W (2019) Isoelectric points of proteins at the air/liquid interface and in solution. Langmuir 35:5004–5012

    CAS  PubMed  Google Scholar 

  66. Hosseinpour S, Roeters SJ, Bonn M, Peukert W, Woutersen S, Weidner T (2020) Structure and dynamics of interfacial peptides and proteins from vibrational sum-frequency generation spectroscopy. Chem Rev 120:3420–3465

    CAS  PubMed  Google Scholar 

  67. Charbgoo F, Nejabat M, Abnous K, Soltani F, Taghdisi SM, Alibolandi M, Thomas Shier W, Steele TWJ, Ramezani M (2018) Gold nanoparticle should understand protein corona for being a clinical nanomaterial. J Control Release 272:39–53

    CAS  PubMed  Google Scholar 

  68. Rahimi M, Ng E-P, Bakhtiari K et al (2015) Zeolite nanoparticles for selective sorption of plasma proteins. Sci Reports 5:1–12

    Google Scholar 

  69. Hu W, Peng C, Lv M, Li X, Zhang Y, Chen N, Fan C, Huang Q (2011) Protein corona-mediated mitigation of cytotoxicity of graphene oxide. ACS Nano 5:3693–3700

    CAS  PubMed  Google Scholar 

  70. Tenzer S, Docter D, Kuharev J, Musyanovych A, Fetz V, Hecht R, Schlenk F, Fischer D, Kiouptsi K, Reinhardt C, Landfester K, Schild H, Maskos M, Knauer SK, Stauber RH (2013) Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat Nanotechnol 8:772–781

    CAS  PubMed  Google Scholar 

  71. Mahmoudi M, Bertrand N, Zope H, Farokhzad OC (2016) Emerging understanding of the protein corona at the nano-bio interfaces. Nano Today 11:817–832

    CAS  Google Scholar 

  72. Karakoti AS, Das S, Thevuthasan S, Seal S (2011) PEGylated inorganic nanoparticles. Angew Chem Int Ed Engl 50:1980–1994

    CAS  PubMed  Google Scholar 

  73. Jokerst JV, Lobovkina T, Zare RN, Gambhir SS (2011) Nanoparticle PEGylation for imaging and therapy. Nanomedicine 6:715–728

    CAS  PubMed  Google Scholar 

  74. Dai Q, Walkey C, Chan WC (2014) Polyethylene glycol backfilling mitigates the negative impact of the protein corona on nanoparticle cell targeting. Angew Chem Int Ed Engl 53:5093–5096

    CAS  PubMed  Google Scholar 

  75. Mirshafiee V, Kim R, Park S, Mahmoudi M, Kraft ML (2016) Impact of protein pre-coating on the protein corona composition and nanoparticle cellular uptake. Biomaterials 75:295–304

    CAS  PubMed  Google Scholar 

  76. Safavi-Sohi R, Maghari S, Raoufi M, Jalali SA, Hajipour MJ, Ghassempour A, Mahmoudi M (2016) Bypassing protein corona issue on active targeting: zwitterionic coatings dictate specific interactions of targeting moieties and cell receptors. ACS Appl Mat Interfaces 8:22808–22818

    CAS  Google Scholar 

  77. Caracciolo G, Safavi-Sohi R, Malekzadeh R, Poustchi H, Vasighi M, Zenezini Chiozzi R, Capriotti AL, Laganà A, Hajipour M, di Domenico M, di Carlo A, Caputo D, Aghaverdi H, Papi M, Palmieri V, Santoni A, Palchetti S, Digiacomo L, Pozzi D, Suslick KS, Mahmoudi M (2019) Disease-specific protein corona sensor arrays may have disease detection capacity. Nanoscale Horizons 4:1063–1076

    CAS  Google Scholar 

  78. Hajipour MJ, Laurent S, Aghaie A, Rezaee F, Mahmoudi M (2014) Personalized protein coronas: a “key” factor at the nanobiointerface. Biomater Sci 2:1210–1221

    CAS  PubMed  Google Scholar 

  79. Hajipour MJ, Raheb J, Akhavan O, Arjmand S, Mashinchian O, Rahman M, Abdolahad M, Serpooshan V, Laurent S, Mahmoudi M (2015) Personalized disease-specific protein corona influences the therapeutic impact of graphene oxide. Nanoscale 7:8978–8994

    CAS  PubMed  Google Scholar 

  80. Caputo D, Caracciolo G (2020) Nanoparticle-enabled blood tests for early detection of pancreatic ductal adenocarcinoma. Cancer Let 470:191–196

    CAS  Google Scholar 

  81. Barui AK, Oh JY, Jana B, Kim C, Ryu JH (2020) Cancer-targeted nanomedicine: overcoming the barrier of the protein corona. Adv Therapeutics 3:1900124

    Google Scholar 

  82. Quagliarini E, Di Santo R, Pozzi D, Caracciolo G (2020) Protein corona-enabled serological tests for early stage cancer detection. Sensors Int 1:100025

    Google Scholar 

  83. Colapicchioni V, Tilio M, Digiacomo L, Gambini V, Palchetti S, Marchini C, Pozzi D, Occhipinti S, Amici A, Caracciolo G (2016) Personalized liposome–protein corona in the blood of breast, gastric and pancreatic cancer patients. Int J Biochem Cell Biol 75:180–187

    CAS  PubMed  Google Scholar 

  84. Lazarovits J, Chen YY, Song F et al (2018) Synthesis of patient-specific nanomaterials. Nano Let 19:116–123

    Google Scholar 

  85. Hadjidemetriou M, Al-Ahmady Z, Buggio M, Swift J, Kostarelos K (2019) A novel scavenging tool for cancer biomarker discovery based on the blood-circulating nanoparticle protein corona. Biomaterials 188:118–129

    CAS  PubMed  Google Scholar 

  86. Digiacomo L, Jafari-Khouzani K, Palchetti S, Pozzi D, Capriotti AL, Laganà A, Zenezini Chiozzi R, Caputo D, Cascone C, Coppola R, Flammia G, Altomare V, Grasso A, Mahmoudi M, Caracciolo G (2020) A protein corona sensor array detects breast and prostate cancers. Nanoscale 12:16697–16704

    CAS  PubMed  Google Scholar 

  87. Hajipour MJ, Ghasemi F, Aghaverdi H, Raoufi M, Linne U, Atyabi F, Nabipour I, Azhdarzadeh M, Derakhshankhah H, Lotfabadi A, Bargahi A, Alekhamis Z, Aghaie A, Hashemi E, Tafakhori A, Aghamollaii V, Mashhadi MM, Sheibani S, Vali H, Mahmoudi M (2017) Sensing of Alzheimer’s disease and multiple sclerosis using nano-bio interfaces. J Alzheimers Dis 59:1187–1202

    CAS  PubMed  Google Scholar 

  88. Gao J, Lin L, Wei A, Sepúlveda MS (2017) Protein corona analysis of silver nanoparticles exposed to fish plasma. Environ Sci Technol Lett 4:174–179

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Hayashi Y, Miclaus T, Murugadoss S et al (2017) Female versus male biological identities of nanoparticles determine the interaction with immune cells in fish. Environ Sci: Nano 4:895–906

    CAS  Google Scholar 

  90. Foroozandeh P, Aziz AA, Mahmoudi M (2019) Effect of cell age on uptake and toxicity of nanoparticles: the overlooked factor at the nanobio interface. ACS Appl Mat Interfaces 11:39672–39687

    CAS  Google Scholar 

Download references

Funding

This work was supported in part by R01CA135650 to A.M.

Author information

Author notes

  1. Morteza Mahmoudi and Anna Moore contributed equally to this work.

Affiliations

  1. Precision Health Program, Michigan State University, East Lansing, MI, 48823, USA

    Morteza Mahmoudi & Anna Moore

  2. Department of Radiology, College of Human Medicine, Michigan State University, East Lansing, MI, 48823, USA

    Morteza Mahmoudi & Anna Moore

Authors
  1. Morteza Mahmoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.M. participated in the conception and outline of the review as well as in manuscript writing. A.M. participated in literature search and analysis as well as in manuscript writing. Both authors accept responsibility and accountability for published work.

Corresponding authors

Correspondence to Morteza Mahmoudi or Anna Moore.

Ethics declarations

Conflict of Interest

The authors declared that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mahmoudi, M., Moore, A. Implications of Biomolecular Corona for Molecular Imaging. Mol Imaging Biol 23, 1–10 (2021). https://doi.org/10.1007/s11307-020-01559-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11307-020-01559-9

Key words

  • Molecular imaging
  • Nanoparticle
  • Biomolecular corona
  • Targeting