Cited by 139

The DOI matches its Crossref record; 17 of the 17 references it cites were found in a registry or an index.

iRGD Peptide as a Tumor-Penetrating Enhancer for Tumor-Targeted Drug Delivery

Kang, Sujin, Lee, Sooyeun, Park, Soyeun·2020·Polymers

Abstract

The unique structure and physiology of a tumor microenvironment impede intra-tumoral penetration of chemotherapeutic agents. A novel iRGD peptide that exploits the tumor microenvironment can activate integrin-dependent binding to tumor vasculatures and neuropilin-1 (NRP-1)-dependent transport to tumor tissues. Recent studies have focused on its dual-targeting ability to achieve enhanced penetration of chemotherapeutics for the efficient eradication of cancer cells. Both the covalent conjugation and the co-administration of iRGD with chemotherapeutic agents and engineered delivery vehicles have been explored. Interestingly, the iRGD-mediated drug delivery also enhances penetration through the blood–brain barrier (BBB). Recent studies have shown its synergistic effect with BBB disruptive techniques. The efficacy of immunotherapy involving immune checkpoint blockades has also been amplified by using iRGD as a targeting moiety. In this review, we presented the recent advances in iRGD technology, focusing on cancer treatment modalities, including the current clinical trials using iRGD. The iRGD-mediated nano-carrier system could serve as a promising strategy in drug delivery to the deeper tumor regions, and be combined with various therapeutic interventions due to its novel targeting ability.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/polym12091906

Cites

17 of 17 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Show all 17 references

Research works printed but not linked: 191

  1. Jung, 2019, Cancer Statistics in Korea: Incidence, Mortality, Survival, and Prevalence in 2016, Cancer Res. Treat., 51, 417, 10.4143/crt.2019.138 · DOI · Paper page
  2. White, 2014, Age and cancer risk: A potentially modifiable relationship, Am. J. Prev. Med., 46, S7, 10.1016/j.amepre.2013.10.029 · DOI · Paper page
  3. Zhang, 2011, A tumor-penetrating peptide modification enhances the antitumor activity of endostatin in vivo, Anticancer Drugs, 22, 409, 10.1097/CAD.0b013e328342050d · DOI
  4. Paydar, 2015, An in vitro study on the effect of vinca alkaloid, vinorelbine, on chromatin histone, HMGB proteins and induction of apoptosis in mice non-adherent bone marrow cells, Drug Chem. Toxicol., 38, 220, 10.3109/01480545.2014.933347 · DOI
  5. Nyongesa, 2018, Chemotherapeutic resistance: A nano-mechanical point of view, Biol. Chem., 399, 1433, 10.1515/hsz-2018-0274 · DOI
  6. Hambley, 2009, Is anticancer drug development heading in the right direction?, Cancer Res., 69, 1259, 10.1158/0008-5472.CAN-08-3786 · DOI
  7. Bissell, 2001, Putting tumours in context, Nat. Rev. Cancer, 1, 46, 10.1038/35094059 · DOI · Paper page
  8. Mueller, 2004, Friends or foes—Bipolar effects of the tumour stroma in cancer, Nat. Rev. Cancer, 4, 839, 10.1038/nrc1477 · DOI
  9. Madara, 1998, Regulation of the movement of solutes across tight junctions, Annu. Rev. Physiol., 60, 143, 10.1146/annurev.physiol.60.1.143 · DOI
  10. Harada, 1996, Abnormal desmoglein expression by squamous cell carcinoma cells, Acta Derm. Venereol., 76, 417, 10.2340/0001555576417420 · DOI
  11. Biedermann, 2005, Desmoglein 2 is expressed abnormally rather than mutated in familial and sporadic gastric cancer, J. Pathol., 207, 199, 10.1002/path.1821 · DOI
  12. Pluen, 2001, Role of tumor-host interactions in interstitial diffusion of macromolecules: Cranial vs. subcutaneous tumors, Proc. Natl. Acad. Sci. USA, 98, 4628, 10.1073/pnas.081626898 · DOI
  13. Jain, 1990, Vascular and interstitial barriers to delivery of therapeutic agents in tumors, Cancer Metastasis Rev., 9, 253, 10.1007/BF00046364 · DOI
  14. Wenning, 1999, Coupled cellular trafficking and diffusional limitations in delivery of immunotoxins to multicell tumor spheroids, Biotechnol. Bioeng., 62, 562, 10.1002/(SICI)1097-0290(19990305)62:5<562::AID-BIT8>3.0.CO;2-4 · DOI
  15. Kuh, 1999, Determinants of paclitaxel penetration and accumulation in human solid tumor, J. Pharmacol. Exp. Ther., 290, 871
  16. Huang, 2005, Cell tension, matrix mechanics, and cancer development, Cancer Cell, 8, 175, 10.1016/j.ccr.2005.08.009 · DOI
  17. Levental, 2009, Matrix crosslinking forces tumor progression by enhancing integrin signaling, Cell, 139, 891, 10.1016/j.cell.2009.10.027 · DOI · Paper page
  18. Lopez, 2011, In situ force mapping of mammary gland transformation, Integr. Biol., 3, 910, 10.1039/c1ib00043h · DOI
  19. Netti, 2000, Role of extracellular matrix assembly in interstitial transport in solid tumors, Cancer Res., 60, 2497
  20. Brown, 2004, Measurement of macromolecular diffusion coefficients in human tumors, Microvasc. Res., 67, 231, 10.1016/j.mvr.2004.02.001 · DOI
  21. Matsumura, 1986, A new concept for macromolecular therapeutics in cancer chemotherapy: Mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs, Cancer Res., 46, 6387
  22. Maeda, 2001, Mechanism of tumor-targeted delivery of macromolecular drugs, including the EPR effect in solid tumor and clinical overview of the prototype polymeric drug SMANCS, J. Control. Release, 74, 47, 10.1016/S0168-3659(01)00309-1 · DOI
  23. Maeda, 2009, Polymeric drugs for efficient tumor-targeted drug delivery based on EPR-effect, Eur. J. Pharm. Biopharm., 71, 409, 10.1016/j.ejpb.2008.11.010 · DOI
  24. Torchilin, 2000, Drug targeting, Eur. J. Pharm. Sci., 11, S81, 10.1016/S0928-0987(00)00166-4 · DOI
  25. Bae, 2009, Drug targeting and tumor heterogeneity, J. Control. Release, 133, 2, 10.1016/j.jconrel.2008.09.074 · DOI
  26. Gabizon, 1994, Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes, Cancer Res., 54, 987
  27. Adams, 2001, High affinity restricts the localization and tumor penetration of single-chain fv antibody molecules, Cancer Res., 61, 4750
  28. Gosk, 2008, VCAM-1 directed immunoliposomes selectively target tumor vasculature in vivo, Biochim. Biophys. Acta, 1778, 854, 10.1016/j.bbamem.2007.12.021 · DOI
  29. Lammers, 2008, Tumour-targeted nanomedicines: Principles and practice, Br. J. Cancer, 99, 392, 10.1038/sj.bjc.6604483 · DOI
  30. Danhier, 2010, To exploit the tumor microenvironment: Passive and active tumor targeting of nanocarriers for anti-cancer drug delivery, J. Control. Release, 148, 135, 10.1016/j.jconrel.2010.08.027 · DOI
  31. Bae, 2011, Targeted drug delivery to tumors: Myths, reality and possibility, J. Control. Release, 153, 198, 10.1016/j.jconrel.2011.06.001 · DOI
  32. Choi, 2013, Strategies to increase drug penetration in solid tumors, Front. Oncol., 3, 193, 10.3389/fonc.2013.00193 · DOI
  33. Summers, 2007, Relaxin receptors—New drug targets for multiple disease states, Curr. Drug Targets, 8, 91, 10.2174/138945007779315650 · DOI
  34. Amento, 1985, Influences of gamma interferon on synovial fibroblast-like cells. Ia induction and inhibition of collagen synthesis, J. Clin. Investig., 76, 837, 10.1172/JCI112041 · DOI
  35. Kim, 2006, Relaxin expression from tumor-targeting adenoviruses and its intratumoral spread, apoptosis induction, and efficacy, J. Natl. Cancer Inst., 98, 1482, 10.1093/jnci/djj397 · DOI
  36. Silvertown, 2006, H2 relaxin overexpression increases in vivo prostate xenograft tumor growth and angiogenesis, Int. J. Cancer, 118, 62, 10.1002/ijc.21288 · DOI
  37. Binder, 2002, Relaxin enhances in-vitro invasiveness of breast cancer cell lines by up-regulation of matrix metalloproteases, Mol. Hum. Reprod, 8, 789, 10.1093/molehr/8.9.789 · DOI
  38. Wang, 2011, Multimerization of adenovirus serotype 3 fiber knob domains is required for efficient binding of virus to desmoglein 2 and subsequent opening of epithelial junctions, J. Virol., 85, 6390, 10.1128/JVI.00514-11 · DOI
  39. Beyer, 2011, Epithelial junction opener JO-1 improves monoclonal antibody therapy of cancer, Cancer Res., 71, 7080, 10.1158/0008-5472.CAN-11-2009 · DOI
  40. Wang, 2011, Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14, Nat. Med., 17, 96, 10.1038/nm.2270 · DOI
  41. Beyer, 2012, Coadministration of epithelial junction opener JO-1 improves the efficacy and safety of chemotherapeutic drugs, Clin. Cancer Res., 18, 3340, 10.1158/1078-0432.CCR-11-3213 · DOI
  42. Li, 2019, Smart Nanotherapeutic Targeting of Tumor Vasculature, Acc. Chem. Res., 52, 2703, 10.1021/acs.accounts.9b00283 · DOI
  43. Zuo, 2014, The effect of superparamagnetic iron oxide with iRGD peptide on the labeling of pancreatic cancer cells in vitro: A preliminary study, BioMed Res. Int., 2014, 852352, 10.1155/2014/852352 · DOI
  44. Yin, 2017, iRGD as a tumorpenetrating peptide for cancer therapy (Review), Mol. Med. Rep., 15, 2925, 10.3892/mmr.2017.6419 · DOI
  45. Hu, 2018, Co-administration of iRGD with peptide HPRP-A1 to improve anticancer activity and membrane penetrability, Sci. Rep., 8, 2274, 10.1038/s41598-018-20715-4 · DOI
  46. Sugahara, 2015, A tumor-penetrating peptide enhances circulation-independent targeting of peritoneal carcinomatosis, J. Control. Release, 212, 59, 10.1016/j.jconrel.2015.06.009 · DOI
  47. Arap, 1998, Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model, Science, 279, 377, 10.1126/science.279.5349.377 · DOI
  48. Sipkins, 1998, Detection of tumor angiogenesis in vivo by alphaVbeta3-targeted magnetic resonance imaging, Nat. Med., 4, 623, 10.1038/nm0598-623 · DOI
  49. Sugahara, 2009, Tissue-penetrating delivery of compounds and nanoparticles into tumors, Cancer Cell, 16, 510, 10.1016/j.ccr.2009.10.013 · DOI
  50. Hoffman, 2003, Progressive vascular changes in a transgenic mouse model of squamous cell carcinoma, Cancer Cell, 4, 383, 10.1016/S1535-6108(03)00273-3 · DOI
  51. Sugahara, 2010, Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs, Science, 328, 1031, 10.1126/science.1183057 · DOI
  52. Teesalu, 2009, C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration, Proc. Natl. Acad. Sci. USA, 106, 16157, 10.1073/pnas.0908201106 · DOI · Paper page
  53. Calderwood, 2004, Integrin activation, J. Cell Sci., 117, 657, 10.1242/jcs.01014 · DOI
  54. Nieberler, M., Reuning, U., Reichart, F., Notni, J., Wester, H.J., Schwaiger, M., Weinmuller, M., Rader, A., Steiger, K., and Kessler, H. (2017). Exploring the Role of RGD-Recognizing Integrins in Cancer. Cancers, 9. · DOI
  55. Huveneers, 2009, Adhesion signaling—Crosstalk between integrins, Src and Rho, J. Cell Sci., 122, 1059, 10.1242/jcs.039446 · DOI
  56. Schittenhelm, 2013, Comparing the expression of integrins alphavbeta3, alphavbeta5, alphavbeta6, alphavbeta8, fibronectin and fibrinogen in human brain metastases and their corresponding primary tumors, Int. J. Clin. Exp. Pathol., 6, 2719
  57. Pytela, 1985, Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor, Cell, 40, 191, 10.1016/0092-8674(85)90322-8 · DOI
  58. Boger, 2015, Integrins alphavbeta3 and alphavbeta5 as prognostic, diagnostic, and therapeutic targets in gastric cancer, Gastric Cancer, 18, 784, 10.1007/s10120-014-0435-2 · DOI
  59. Schnell, 2008, Expression of integrin alphavbeta3 in gliomas correlates with tumor grade and is not restricted to tumor vasculature, Brain Pathol., 18, 378, 10.1111/j.1750-3639.2008.00137.x · DOI
  60. Boger, 2014, Integrins and their ligands are expressed in non-small cell lung cancer but not correlated with parameters of disease progression, Virchows Arch., 464, 69, 10.1007/s00428-013-1506-1 · DOI
  61. Hosotani, 2002, Expression of integrin alphaVbeta3 in pancreatic carcinoma: Relation to MMP-2 activation and lymph node metastasis, Pancreas, 25, e30, 10.1097/00006676-200208000-00021 · DOI
  62. Hess, 2014, Correlation between the expression of integrins in prostate cancer and clinical outcome in 1284 patients, Ann. Diagn Pathol., 18, 343, 10.1016/j.anndiagpath.2014.09.001 · DOI
  63. Berghoff, 2014, Alphavbeta3, alphavbeta5 and alphavbeta6 integrins in brain metastases of lung cancer, Clin. Exp. Metastasis, 31, 841, 10.1007/s10585-014-9675-0 · DOI
  64. Xiong, 2002, Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand, Science, 296, 151, 10.1126/science.1069040 · DOI
  65. Jusino, 2007, Structural basis for ligand and heparin binding to neuropilin B domains, Proc. Natl. Acad. Sci. USA, 104, 6152, 10.1073/pnas.0700043104 · DOI
  66. Haspel, 2011, Binding of a C-end rule peptide to the neuropilin-1 receptor: A molecular modeling approach, Biochemistry, 50, 1755, 10.1021/bi101662j · DOI
  67. Koivunen, 1995, Phage libraries displaying cyclic peptides with different ring sizes: Ligand specificities of the RGD-directed integrins, Biotechnology, 13, 265
  68. Salikhova, 2008, Vascular endothelial growth factor and semaphorin induce neuropilin-1 endocytosis via separate pathways, Circ. Res., 103, e71, 10.1161/CIRCRESAHA.108.183327 · DOI · Paper page
  69. Feron, O. (2010). Tumor-penetrating peptides: A shift from magic bullets to magic guns. Sci. Transl. Med., 2. · DOI
  70. Takagi, 1991, The A5 antigen, a candidate for the neuronal recognition molecule, has homologies to complement components and coagulation factors, Neuron, 7, 295, 10.1016/0896-6273(91)90268-5 · DOI
  71. Neufeld, 2008, The semaphorins: Versatile regulators of tumour progression and tumour angiogenesis, Nat. Rev. Cancer, 8, 632, 10.1038/nrc2404 · DOI
  72. Gaur, 2009, Role of class 3 semaphorins and their receptors in tumor growth and angiogenesis, Clin. Cancer Res., 15, 6763, 10.1158/1078-0432.CCR-09-1810 · DOI
  73. Kitsukawa, 1995, Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs, Development, 121, 4309, 10.1242/dev.121.12.4309 · DOI
  74. Kawasaki, 1999, A requirement for neuropilin-1 in embryonic vessel formation, Development, 126, 4895, 10.1242/dev.126.21.4895 · DOI
  75. Soker, 1998, Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor, Cell, 92, 735, 10.1016/S0092-8674(00)81402-6 · DOI
  76. Poon, 2001, Clinical implications of circulating angiogenic factors in cancer patients, J. Clin. Oncol., 19, 1207, 10.1200/JCO.2001.19.4.1207 · DOI
  77. Bachelder, 2001, Vascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells, Cancer Res., 61, 5736
  78. Zhang, 2016, The prognostic value of neuropilin-1 in various cancers: A meta-analysis, Int. J. Clin. Exp. Med., 9, 13942
  79. Akashi, 2014, Anticancer effects of gemcitabine are enhanced by co-administered iRGD peptide in murine pancreatic cancer models that overexpressed neuropilin-1, Br. J. Cancer, 110, 1481, 10.1038/bjc.2014.49 · DOI
  80. Seo, 2020, Relationship between neuropilin-1 expression and prognosis, according to gastric cancer histology, J. Mol. Histol., 51, 199, 10.1007/s10735-020-09870-z · DOI
  81. Hanahan, 1996, Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis, Cell, 86, 353, 10.1016/S0092-8674(00)80108-7 · DOI · Paper page
  82. Raghunand, 2003, Microenvironmental and cellular consequences of altered blood flow in tumours, Br. J. Radiol., 76, S11, 10.1259/bjr/12913493 · DOI
  83. Carmeliet, 2000, Mechanisms of angiogenesis and arteriogenesis, Nat. Med., 6, 389, 10.1038/74651 · DOI
  84. Desgrosellier, 2010, Integrins in cancer: Biological implications and therapeutic opportunities, Nat. Rev. Cancer, 10, 9, 10.1038/nrc2748 · DOI
  85. Avraamides, 2008, Integrins in angiogenesis and lymphangiogenesis, Nat. Rev. Cancer, 8, 604, 10.1038/nrc2353 · DOI · Paper page
  86. Stollman, 2009, New targeted probes for radioimaging of angiogenesis, Methods, 48, 188, 10.1016/j.ymeth.2009.03.006 · DOI
  87. Wang, 2014, Tumor penetrability and anti-angiogenesis using iRGD-mediated delivery of doxorubicin-polymer conjugates, Biomaterials, 35, 8735, 10.1016/j.biomaterials.2014.06.042 · DOI
  88. Laakkonen, 2002, A tumor-homing peptide with a targeting specificity related to lymphatic vessels, Nat. Med., 8, 751, 10.1038/nm720 · DOI
  89. Alberici, 2013, De novo design of a tumor-penetrating peptide, Cancer Res., 73, 804, 10.1158/0008-5472.CAN-12-1668 · DOI
  90. Xiao, 2020, Cancer Targeted Gene Therapy for Inhibition of Melanoma Lung Metastasis with eIF3i shRNA Loaded Liposomes, Mol. Pharm., 17, 229, 10.1021/acs.molpharmaceut.9b00943 · DOI
  91. Bao, 2020, Cancer-targeted PEDF-DNA therapy for metastatic colorectal cancer, Int. J. Pharm., 576, 118999, 10.1016/j.ijpharm.2019.118999 · DOI
  92. Yan, 2016, Molecular imaging-guided photothermal/photodynamic therapy against tumor by iRGD-modified indocyanine green nanoparticles, J. Control. Release, 224, 217, 10.1016/j.jconrel.2015.12.050 · DOI
  93. Shen, 2014, iRGD conjugated TPGS mediates codelivery of paclitaxel and survivin shRNA for the reversal of lung cancer resistance, Mol. Pharm., 11, 2579, 10.1021/mp400576f · DOI
  94. Wang, 2015, Multifunctional porous silicon nanoparticles for cancer theranostics, Biomaterials, 48, 108, 10.1016/j.biomaterials.2015.01.008 · DOI
  95. Li, 2016, Tumor vascular-targeted co-delivery of anti-angiogenesis and chemotherapeutic agents by mesoporous silica nanoparticle-based drug delivery system for synergetic therapy of tumor, Int. J. Nanomed., 11, 93
  96. Liu, 2017, Targeted drug delivery using iRGD peptide for solid cancer treatment, Mol. Syst. Des. Eng., 2, 370, 10.1039/C7ME00050B · DOI
  97. Miura, 2013, Cyclic RGD-linked polymeric micelles for targeted delivery of platinum anticancer drugs to glioblastoma through the blood-brain tumor barrier, ACS Nano, 7, 8583, 10.1021/nn402662d · DOI
  98. Lu, 2020, An iRGD-conjugated prodrug micelle with blood-brain-barrier penetrability for anti-glioma therapy, Biomaterials, 230, 119666, 10.1016/j.biomaterials.2019.119666 · DOI
  99. Irby, 2017, Lipid-Drug Conjugate for Enhancing Drug Delivery, Mol. Pharm., 14, 1325, 10.1021/acs.molpharmaceut.6b01027 · DOI
  100. Han, 2018, Improvement of cellular uptake of hydrophilic molecule, calcein, formulated by liposome, J. Pharm. Investig., 48, 595, 10.1007/s40005-017-0358-0 · DOI
  101. Song, 2016, Development of a multi-target peptide for potentiating chemotherapy by modulating tumor microenvironment, Biomaterials, 108, 44, 10.1016/j.biomaterials.2016.09.001 · DOI
  102. Wang, 2016, iRGD-mediated reduction-responsive DSPE–PEG/LA–PLGA–TPGS mixed micelles used in the targeted delivery and triggered release of docetaxel in cancer, RSC Adv., 6, 28331, 10.1039/C5RA19814C · DOI
  103. Liu, 2013, Enhanced therapeutic efficacy of iRGD-conjugated crosslinked multilayer liposomes for drug delivery, BioMed Res. Int., 2013, 378380
  104. Yu, 2013, The antitumor activity of a doxorubicin loaded, iRGD-modified sterically-stabilized liposome on B16-F10 melanoma cells: In vitro and in vivo evaluation, Int. J. Nanomed., 8, 2473
  105. Dai, 2015, A comprehensive study of iRGD-modified liposomes with improved chemotherapeutic efficacy on B16 melanoma, Drug Deliv., 22, 10, 10.3109/10717544.2014.903580 · DOI
  106. Chen, 2017, nRGD modified lycobetaine and octreotide combination delivery system to overcome multiple barriers and enhance anti-glioma efficacy, Colloids Surf. B Biointerfaces, 156, 330, 10.1016/j.colsurfb.2017.05.038 · DOI
  107. Nie, 2014, Targeting peptide iRGD-conjugated amphiphilic chitosan-co-PLA/DPPE drug delivery system for enhanced tumor therapy, J. Mater. Chem. B, 2, 3232, 10.1039/c3tb21744b · DOI
  108. Zhang, 2019, Multitargeted Nanoparticles Deliver Synergistic Drugs across the Blood-Brain Barrier to Brain Metastases of Triple Negative Breast Cancer Cells and Tumor-Associated Macrophages, Adv. Health Mater., 8, e1900543, 10.1002/adhm.201900543 · DOI
  109. Chen, 2019, Remarkable Boron Delivery Of iRGD-Modified Polymeric Nanoparticles for Boron Neutron Capture Therapy, Int. J. Nanomed., 14, 8161, 10.2147/IJN.S214224 · DOI
  110. Xie, 2019, Transarterial Infusion of iRGD-Modified ZrO(2) Nanoparticles with Lipiodol Improves the Tissue Distribution of Doxorubicin and Its Antitumor Efficacy, J. Vasc. Interv. Radiol., 30, 2026, 10.1016/j.jvir.2019.04.014 · DOI
  111. Hunt, 2016, iRGD peptide conjugation potentiates intraperitoneal tumor delivery of paclitaxel with polymersomes, Biomaterials, 104, 247, 10.1016/j.biomaterials.2016.07.023 · DOI
  112. Zhu, 2011, The effect of hydrophilic chain length and iRGD on drug delivery from poly(ε-caprolactone)-poly(N-vinylpyrrolidone) nanoparticles, Biomaterials, 32, 9525, 10.1016/j.biomaterials.2011.08.072 · DOI
  113. Kang, 2019, Modular Engineering of Targeted Dual-Drug Nanoassemblies for Cancer Chemoimmunotherapy, ACS Appl. Mater. Interfaces, 11, 36371, 10.1021/acsami.9b11881 · DOI
  114. Liu, 2017, iRGD-mediated core-shell nanoparticles loading carmustine and O(6)-benzylguanine for glioma therapy, J. Drug Target., 25, 235, 10.1080/1061186X.2016.1238091 · DOI
  115. Bessone, 2019, iRGD-guided tamoxifen polymersomes inhibit estrogen receptor transcriptional activity and decrease the number of breast cancer cells with self-renewing capacity, J. Nanobiotechnol., 17, 1
  116. Gao, 2017, iRGD-modified lipid-polymer hybrid nanoparticles loaded with isoliquiritigenin to enhance anti-breast cancer effect and tumor-targeting ability, Int. J. Nanomed., 12, 4147, 10.2147/IJN.S134148 · DOI
  117. Lee, 2019, Cyclic iRGD peptide as a dual-functional on–off gatekeeper of mesoporous nanocontainers for targeting NRP-1 and selective drug release triggered by conformational conversion, New J. Chem., 43, 1517, 10.1039/C8NJ04649B · DOI
  118. Su, 2013, iRGD-coupled responsive fluorescent nanogel for targeted drug delivery, Biomaterials, 34, 3523, 10.1016/j.biomaterials.2013.01.083 · DOI
  119. Zhang, 2020, Photosensitizer-loaded cell membrane biomimetic nanoparticles for enhanced tumor synergetic targeted therapy, RSC Adv., 10, 9378, 10.1039/C9RA08926H · DOI
  120. Carvalho, 2019, Radiation-Induced Targeted Nanoparticle-Based Gene Delivery for Brain Tumor Therapy, ACS Nano, 13, 4028, 10.1021/acsnano.8b08177 · DOI
  121. Jin, 2016, Core-shell nanocarriers with high paclitaxel loading for passive and active targeting, Sci. Rep., 6, 27559, 10.1038/srep27559 · DOI
  122. Gu, 2013, The influence of the penetrating peptide iRGD on the effect of paclitaxel-loaded MT1-AF7p-conjugated nanoparticles on glioma cells, Biomaterials, 34, 5138, 10.1016/j.biomaterials.2013.03.036 · DOI
  123. Zhong, 2019, Co-Administration of iRGD Enhances Tumor-Targeted Delivery and Anti-Tumor Effects of Paclitaxel-Loaded PLGA Nanoparticles for Colorectal Cancer Treatment, Int. J. Nanomed., 14, 8543, 10.2147/IJN.S219820 · DOI
  124. Deng, 2018, Co-administration of biocompatible self-assembled polylactic acid-hyaluronic acid block copolymer nanoparticles with tumor-penetrating peptide-iRGD for metastatic breast cancer therapy, J. Mater. Chem. B, 6, 3163, 10.1039/C8TB00319J · DOI
  125. Liu, 2017, Tumor-penetrating peptide enhances transcytosis of silicasome-based chemotherapy for pancreatic cancer, J. Clin. Investig., 127, 2007, 10.1172/JCI92284 · DOI
  126. Deng, 2017, Coadministration of Oligomeric Hyaluronic Acid-Modified Liposomes with Tumor-Penetrating Peptide-iRGD Enhances the Antitumor Efficacy of Doxorubicin against Melanoma, ACS Appl. Mater. Interfaces, 9, 1280, 10.1021/acsami.6b13738 · DOI
  127. Yu, 2015, Co-administration of iRGD enhancing the anticancer efficacy of cisplatin-loaded polypeptide nanoparticles, J. Control. Release, 213, e145, 10.1016/j.jconrel.2015.05.246 · DOI
  128. Cun, 2015, A Novel Strategy through Combining iRGD Peptide with Tumor-Microenvironment-Responsive and Multistage Nanoparticles for Deep Tumor Penetration, ACS Appl. Mater. Interfaces, 7, 27458, 10.1021/acsami.5b09391 · DOI
  129. Umeshappa, 2018, Comment on “Coadministration of iRGD with Multistage Responsive Nanoparticles Enhanced Tumor Targeting and Penetration Abilities for Breast Cancer Therapy”, ACS Appl. Mater. Interfaces, 10, 38659, 10.1021/acsami.8b11346 · DOI
  130. Zhang, Q., Zhang, Y., Li, K., Wang, H., Li, H., and Zheng, J. (2015). A Novel Strategy to Improve the Therapeutic Efficacy of Gemcitabine for Non-Small Cell Lung Cancer by the Tumor-Penetrating Peptide iRGD. PLoS ONE, 10. · DOI
  131. Zhang, 2016, Tumor-penetration and antitumor efficacy of cetuximab are enhanced by co-administered iRGD in a murine model of human NSCLC, Oncol. Lett., 12, 3241, 10.3892/ol.2016.5081 · DOI
  132. Fadeev, R., Chekanov, A., Solovieva, M., Bezborodova, O., Nemtsova, E., Dolgikh, N., Fadeeva, I., Senotov, A., Kobyakova, M., and Evstratova, Y. (2019). Improved Anticancer Effect of Recombinant Protein izTRAIL Combined with Sorafenib and Peptide iRGD. Int. J. Mol. Sci., 20. · DOI
  133. Zhang, 2020, Antitumor Activity of Thermosensitive Hydrogels Packaging Gambogic Acid Nanoparticles and Tumor-Penetrating Peptide iRGD Against Gastric Cancer, Int. J. Nanomed., 15, 735, 10.2147/IJN.S231448 · DOI
  134. Saad, A.M., Turk, T., Al-Husseini, M.J., and Abdel-Rahman, O. (2018). Trends in pancreatic adenocarcinoma incidence and mortality in the United States in the last four decades; a SEER-based study. BMC Cancer, 18. · DOI
  135. Khalaf, N., El-Serag, H.B., Abrams, H.R., and Thrift, A.P. (2020). Burden of Pancreatic Cancer—From Epidemiology to Practice. Clin. Gastroenterol. Hepatol. · DOI · Paper page
  136. Rahib, 2014, Projecting cancer incidence and deaths to 2030: The unexpected burden of thyroid, liver, and pancreas cancers in the United States, Cancer Res., 74, 2913, 10.1158/0008-5472.CAN-14-0155 · DOI · Paper page
  137. Oberstein, 2013, Pancreatic cancer: Why is it so hard to treat?, Ther. Adv. Gastroenterol., 6, 321, 10.1177/1756283X13478680 · DOI
  138. Frese, 2012, Nab-Paclitaxel potentiates gemcitabine activity by reducing cytidine deaminase levels in a mouse model of pancreatic cancer, Cancer Discov., 2, 260, 10.1158/2159-8290.CD-11-0242 · DOI
  139. Ramanathan, 2011, Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: A phase I/II trial, J. Clin. Oncol., 29, 4548, 10.1200/JCO.2011.36.5742 · DOI
  140. Fukahi, 2004, Aberrant expression of neuropilin-1 and -2 in human pancreatic cancer cells, Clin. Cancer Res., 10, 581, 10.1158/1078-0432.CCR-0930-03 · DOI
  141. Wey, 2005, Overexpression of neuropilin-1 promotes constitutive MAPK signalling and chemoresistance in pancreatic cancer cells, Br. J. Cancer, 93, 233, 10.1038/sj.bjc.6602663 · DOI
  142. Fukasawa, 2007, Neuropilin-1 interacts with integrin beta1 and modulates pancreatic cancer cell growth, survival and invasion, Cancer Biol. Ther., 6, 1173, 10.4161/cbt.6.8.4363 · DOI
  143. Matkar, 2016, Novel regulatory role of neuropilin-1 in endothelial-to-mesenchymal transition and fibrosis in pancreatic ductal adenocarcinoma, Oncotarget, 7, 69489, 10.18632/oncotarget.11060 · DOI
  144. Slaney, 2014, Trafficking of T cells into tumors, Cancer Res., 74, 7168, 10.1158/0008-5472.CAN-14-2458 · DOI
  145. Sun, 2019, Tumor targeting DVDMS-nanoliposomes for an enhanced sonodynamic therapy of gliomas, Biomater. Sci., 7, 985, 10.1039/C8BM01187G · DOI
  146. Martin, 2000, Exotoxins of Staphylococcus aureus, Clin. Microbiol. Rev., 13, 16, 10.1128/CMR.13.1.16 · DOI
  147. Song, 2020, An iRGD peptide fused superantigen mutant induced tumor-targeting and T lymphocyte infiltrating in cancer immunotherapy, Int. J. Pharm., 586, 119498, 10.1016/j.ijpharm.2020.119498 · DOI
  148. Ricci, 2006, Chemotherapeutic approaches for targeting cell death pathways, Oncologist, 11, 342, 10.1634/theoncologist.11-4-342 · DOI
  149. Li, 2005, Inactivation of nuclear factor κB by soy isoflavone genistein contributes to increased apoptosis induced by chemotherapeutic agents in human cancer cells, Cancer Res., 65, 6934, 10.1158/0008-5472.CAN-04-4604 · DOI
  150. Ferreira, 2015, Antitumor immunity triggered by melphalan is potentiated by melanoma cell surface–associated calreticulin, Cancer Res., 75, 1603, 10.1158/0008-5472.CAN-14-2089 · DOI
  151. Ding, 2014, Chemotherapy-induced myeloid suppressor cells and antitumor immunity: The Janus face of chemotherapy in immunomodulation, Oncoimmunology, 3, e954471, 10.4161/21624011.2014.954471 · DOI
  152. Pruneri, 2016, Tumor-infiltrating lymphocytes (TILs) are a powerful prognostic marker in patients with triple-negative breast cancer enrolled in the IBCSG phase III randomized clinical trial 22-00, Breast Cancer Res. Treat., 158, 323, 10.1007/s10549-016-3863-3 · DOI
  153. Lake, 2005, Immunotherapy and chemotherapy—A practical partnership, Nat. Rev. Cancer, 5, 397, 10.1038/nrc1613 · DOI
  154. Chang, 2013, Dose-dense chemotherapy improves mechanisms of antitumor immune response, Cancer Res., 73, 119, 10.1158/0008-5472.CAN-12-2225 · DOI
  155. Deng, 2017, Inducing Optimal Antitumor Immune Response through Coadministering iRGD with Pirarubicin Loaded Nanostructured Lipid Carriers for Breast Cancer Therapy, Mol. Pharm., 14, 296, 10.1021/acs.molpharmaceut.6b00932 · DOI
  156. Kolishetti, 2010, Engineering of self-assembled nanoparticle platform for precisely controlled combination drug therapy, Proc. Natl. Acad. Sci. USA, 107, 17939, 10.1073/pnas.1011368107 · DOI
  157. Han, 2018, A nanomedicine approach enables co-delivery of cyclosporin A and gefitinib to potentiate the therapeutic efficacy in drug-resistant lung cancer, Signal. Transduct Target. Ther., 3, 16, 10.1038/s41392-018-0019-4 · DOI
  158. Le, 2018, Nano delivery systems and cancer immunotherapy, J. Pharm. Investig., 48, 527, 10.1007/s40005-018-0399-z · DOI
  159. Tran, 2020, Recent advances of nanotechnology for the delivery of anticancer drugs for breast cancer treatment, J. Pharm. Investig., 50, 261, 10.1007/s40005-019-00459-7 · DOI
  160. Park, 2018, Future prospects of immune checkpoint blockade in cancer: From response prediction to overcoming resistance, Exp. Mol. Med., 50, 109, 10.1038/s12276-018-0130-1 · DOI
  161. Kunimasa, K., and Goto, T. (2020). Immunosurveillance and Immunoediting of Lung Cancer: Current Perspectives and Challenges. Int. J. Mol. Sci., 21. · DOI
  162. Schneider, 2006, Reversal of the TCR stop signal by CTLA-4, Science, 313, 1972, 10.1126/science.1131078 · DOI
  163. Walunas, 1994, CTLA-4 can function as a negative regulator of T cell activation, Immunity, 1, 405, 10.1016/1074-7613(94)90071-X · DOI · Paper page
  164. Kwiecien, 2017, Elevated regulatory T cells, surface and intracellular CTLA-4 expression and interleukin-17 in the lung cancer microenvironment in humans, Cancer Immunol. Immunother., 66, 161, 10.1007/s00262-016-1930-6 · DOI
  165. Chemnitz, 2004, SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation, J. Immunol., 173, 945, 10.4049/jimmunol.173.2.945 · DOI · Paper page
  166. Parry, 2005, CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms, Mol. Cell Biol., 25, 9543, 10.1128/MCB.25.21.9543-9553.2005 · DOI · Paper page
  167. Chen, 2016, Regulation of PD-L1: A novel role of pro-survival signalling in cancer, Ann. Oncol., 27, 409, 10.1093/annonc/mdv615 · DOI · Paper page
  168. Rosenberg, 2016, Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: A single-arm, multicentre, phase 2 trial, Lancet, 387, 1909, 10.1016/S0140-6736(16)00561-4 · DOI · Paper page
  169. Pardoll, 2012, The blockade of immune checkpoints in cancer immunotherapy, Nat. Rev. Cancer, 12, 252, 10.1038/nrc3239 · DOI · Paper page
  170. Wei, 2018, Fundamental Mechanisms of Immune Checkpoint Blockade Therapy, Cancer Discov., 8, 1069, 10.1158/2159-8290.CD-18-0367 · DOI · Paper page
  171. Yang, 2019, Immunomodulators targeting the PD-1/PD-L1 protein-protein interaction: From antibodies to small molecules, Med. Res. Rev., 39, 265, 10.1002/med.21530 · DOI
  172. Seidel, 2018, Anti-PD-1 and anti-CTLA-4 therapies in cancer: Mechanisms of action, efficacy, and limitations, Front. Oncol., 8, 86, 10.3389/fonc.2018.00086 · DOI · Paper page
  173. Yang, 2019, Modification of IL-24 by tumor penetrating peptide iRGD enhanced its antitumor efficacy against non-small cell lung cancer, Int. Immunopharmacol., 70, 125, 10.1016/j.intimp.2019.02.027 · DOI
  174. Jarvelainen, H., Botta, G.P., De Mendoza, T.H., and Ruoslahti, E. (April, January 29). Co-administration of the iRGD tumor-penetrating peptide improves the tumor immunostimulatory effects of low-dose IL-2. Proceedings of the AACR Annual Meeting, Atlanta, GA, USA.
  175. Zhang, 2018, Nanoparticles That Reshape the Tumor Milieu Create a Therapeutic Window for Effective T-cell Therapy in Solid Malignancies, Cancer Res., 78, 3718, 10.1158/0008-5472.CAN-18-0306 · DOI
  176. Ding, 2019, iRGD synergizes with PD-1 knockout immunotherapy by enhancing lymphocyte infiltration in gastric cancer, Nat. Commun., 10, 1336, 10.1038/s41467-019-09296-6 · DOI
  177. Zhao, 2020, Nanocarrier-based drug combination therapy for glioblastoma, Theranostics, 10, 1355, 10.7150/thno.38147 · DOI
  178. Rubin, 1999, The cell biology of the blood-brain barrier, Annu. Rev. Neurosci., 22, 11, 10.1146/annurev.neuro.22.1.11 · DOI
  179. Luissint, 2012, Guanine nucleotide-binding protein Galphai2: A new partner of claudin-5 that regulates tight junction integrity in human brain endothelial cells, J. Cereb. Blood Flow Metab., 32, 860, 10.1038/jcbfm.2011.202 · DOI
  180. Pardridge, 2012, Drug transport across the blood-brain barrier, J. Cereb. Blood Flow Metab., 32, 1959, 10.1038/jcbfm.2012.126 · DOI · Paper page
  181. Nishio, 1983, Microvascular abnormalities in ethylnitrosourea (ENU)-induced rat brain tumors: Structural basis for altered blood-brain barrier function, Acta Neuropathol., 59, 1, 10.1007/BF00690311 · DOI
  182. Wolburg, 2012, The disturbed blood-brain barrier in human glioblastoma, Mol. Asp. Med., 33, 579, 10.1016/j.mam.2012.02.003 · DOI
  183. Li, 2010, The structure and functions of P-glycoprotein, Curr. Med. Chem., 17, 786, 10.2174/092986710790514507 · DOI
  184. Siegal, 2000, In vivo assessment of the window of barrier opening after osmotic blood-brain barrier disruption in humans, J Neurosurg., 92, 599, 10.3171/jns.2000.92.4.0599 · DOI
  185. Wesseling, 2015, Overcoming the blood-brain tumor barrier for effective glioblastoma treatment, Drug Resist. Updates, 19, 1, 10.1016/j.drup.2015.02.002 · DOI · Paper page
  186. Raymond, 1986, Pharmacological modification of bradykinin induced breakdown of the blood-brain barrier, Can. J. Neurol. Sci., 13, 214, 10.1017/S0317167100036301 · DOI
  187. Vogelbaum, M.A., and Aghi, M.K. (2015). Convection-enhanced delivery for the treatment of glioblastoma. Neuro-Oncology, 17. · DOI
  188. Hamilton, 2015, Nanoparticles coated with the tumor-penetrating peptide iRGD reduce experimental breast cancer metastasis in the brain, J. Mol. Med., 93, 991, 10.1007/s00109-015-1279-x · DOI
  189. Moncelet, D., Bouchaud, V., Mellet, P., Ribot, E., Miraux, S., Franconi, J.M., and Voisin, P. (2013). Cellular density effect on RGD ligand internalization in glioblastoma for MRI application. PLoS ONE, 8. · DOI
  190. Liu, 2014, Surface tailoring of nanoparticles via mixed-charge monolayers and their biomedical applications, Small, 10, 4230, 10.1002/smll.201401440 · DOI
  191. Ruoslahti, 2012, Peptides as targeting elements and tissue penetration devices for nanoparticles, Adv. Mater., 24, 3747, 10.1002/adma.201200454 · DOI

Cited by

Sorted by citations

See all 139

Metadata

Authors
Kang, S., Lee, S., & Park, S.
Venue
Polymers
Publisher
MDPI AG
Published
2020-08-24
Volume
12
Issue
9
Pages
1906
ISSN
2073-4360
Cited by
139
References
17
Language
en
Funders
National Research Foundation of Korea (NRF-2018R1D1A3B07050399, NRF-2016R1A6A1A03011325)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review