Recent progress in LyP-1-based strategies for targeted imaging and therapy

References

• Abulrob A, Corluka S, Blasiak B, et al. (2018). LyP-1 conjugated nanoparticles for magnetic resonance imaging of triple negative breast cancer. Mol Imaging Biol 20:428–35.
   PubMed Web of Science ®Google Scholar
• Bailey DL, Willowson KP. (2014). Quantitative SPECT/CT: SPECT joins PET as a quantitative imaging modality. Eur J Nucl Med Mol Imaging 41:17–25.
   Web of Science ®Google Scholar
• Bickel U, Kang YS, Pardridge WM. (1995). In vivo cleavability of a disulfide-based chimeric opioid peptide in rat brain. Bioconjug Chem 6:211–8.
   PubMed Web of Science ®Google Scholar
• Bjorge JD, Pang A, Fujita DJ. (2017). Delivery of gene targeting siRNAs to breast cancer cells using a multifunctional peptide complex that promotes both targeted delivery and endosomal release. PLoS One 12:e0180578.
   PubMed Web of Science ®Google Scholar
• Casi G, Neri D. (2015). Antibody-drug conjugates and small molecule-drug conjugates: opportunities and challenges for the development of selective anticancer cytotoxic agents. J Med Chem 58:8751–61.
   PubMed Web of Science ®Google Scholar
• David A. (2017). Peptide ligand-modified nanomedicines for targeting cells at the tumor microenvironment. Adv Drug Deliv Rev 119:120–42.
   PubMed Web of Science ®Google Scholar
• Deb TB, Datta K. (1996). Molecular cloning of human fibroblast hyaluronic acid-binding protein confirms its identity with P-32, a protein co-purified with splicing factor SF2. Hyaluronic acid-binding protein as P-32 protein, co-purified with splicing factor SF2. J Biol Chem 271:2206–12.
   PubMed Web of Science ®Google Scholar
• Dedio J, Jahnen-Dechent W, Bachmann M, et al. (1998) The multiligand-binding protein gC1qR, putative C1q receptor, is a mitochondrial protein. J Immunol 160:3534–42.
   Web of Science ®Google Scholar
• Enback J, Laakkonen P. (2007). Tumour-homing peptides: tools for targeting, imaging and destruction. Biochem Soc Trans 35:780–3.
   PubMed Web of Science ®Google Scholar
• Fogal V, Richardson AD, Karmali PP, et al. (2010). Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Mol Cell Biol 30:1303–18.
   PubMed Web of Science ®Google Scholar
• Fogal V, Zhang L, Krajewski S, et al. (2008). Mitochondrial/cell-surface protein p32/gC1qR as a molecular target in tumor cells and tumor stroma. Cancer Res 68:7210–8.
   PubMed Web of Science ®Google Scholar
• Gabizon AA, Patil Y, La-Beck NM. (2016). New insights and evolving role of pegylated liposomal doxorubicin in cancer therapy. Drug Resist Updat 29:90–106.
   PubMed Web of Science ®Google Scholar
• Greco F, Vicent MJ. (2009). Combination therapy: opportunities and challenges for polymer-drug conjugates as anticancer nanomedicines. Adv Drug Deliv Rev 61:1203–13.
   PubMed Web of Science ®Google Scholar
• Gursoy RN, Cevik O. (2014). Design, characterization and in vitro evaluation of SMEDDS containing an anticancer peptide, linear LyP-1. Pharm Dev Technol 19:486–90.
   PubMed Web of Science ®Google Scholar
• Habash RW, Krewski D, Bansal R, et al. (2011). Principles, applications, risks and benefits of therapeutic hyperthermia. Front Biosci (Elite Ed) 3:1169–81.
   PubMedGoogle Scholar
• Hamzah J, Kotamraju VR, Seo JW, et al. (2011). Specific penetration and accumulation of a homing peptide within atherosclerotic plaques of apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 108:7154–9.
   PubMed Web of Science ®Google Scholar
• Herringson TP, Altin JG. (2011). Effective tumor targeting and enhanced anti-tumor effect of liposomes engrafted with peptides specific for tumor lymphatics and vasculature. Int J Pharm 411:206–14.
   PubMed Web of Science ®Google Scholar
• Jiang C, Li X, Yan F, et al. (2011). Microfluidic-assisted formation of multifunctional monodisperse microbubbles for diagnostics and therapeutics. Micro Nano Lett 6:417–21.
   Web of Science ®Google Scholar
• Jiang J, Zhang Y, Krainer AR, et al. (1999). Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein. Proc Natl Acad Sci USA 96:3572–7.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Liu S, Zhang Y, et al. (2017). Magnetic mesoporous nanospheres anchored with LyP-1 as an efficient pancreatic cancer probe. Biomaterials 115:9–18.
   PubMed Web of Science ®Google Scholar
• Karmali PP, Kotamraju VR, Kastantin M, et al. (2009). Targeting of albumin-embedded paclitaxel nanoparticles to tumors. Nanomedicine 5:73–82.
   PubMed Web of Science ®Google Scholar
• Kiessling F, Fokong S, Koczera P, et al. (2012). Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics. J Nucl Med 53:345–8.
   PubMed Web of Science ®Google Scholar
• Kinsella JM, Jimenez RE, Karmali PP, et al. (2011). X-ray computed omography imaging of breast cancer by using targeted peptide-labeled bismuth sulfide nanoparticles. Angew Chem Int Ed Engl 50:12308–11.
   PubMed Web of Science ®Google Scholar
• Koenig W, Khuseyinova N. (2007). Biomarkers of atherosclerotic plaque instability and rupture. Arterioscler Thromb Vasc Biol 27:15–26.
   PubMed Web of Science ®Google Scholar
• Kotamraju VR, Sharma S, Kolhar P, et al. (2015). Increasing tumor accessibility with conjugatable disulfide-bridged tumor-penetrating peptides for cancer diagnosis and treatment. Breast Cancer (Auckl) 9:79–87.
   PubMedGoogle Scholar
• Laakkonen P, Akerman ME, Biliran H, et al. (2004). Antitumor activity of a homing peptide that targets tumor lymphatics and tumor cells. Proc Natl Acad Sci USA 101:9381–6.
   PubMed Web of Science ®Google Scholar
• Laakkonen P, Porkka K, Hoffman JA, et al. (2002). A tumor-homing peptide with a targeting specificity related to lymphatic vessels. Nat Med 8:751–5.
   PubMed Web of Science ®Google Scholar
• Laakkonen P, Zhang L, Ruoslahti E. (2008). Peptide targeting of tumor lymph vessels. Ann NY Acad Sci 1131:37–43.
   PubMed Web of Science ®Google Scholar
• Lai H, Sasaki T, Singh NP. (2005). Targeted treatment of cancer with artemisinin and artemisinin-tagged iron-carrying compounds. Expert Opin Ther Targets 9:995–1007.
   PubMed Web of Science ®Google Scholar
• Lai HC, Singh NP, Sasaki T. (2013). Development of artemisinin compounds for cancer treatment. Invest New Drugs 31:230–46.
   PubMed Web of Science ®Google Scholar
• Laurent S, Saei AA, Behzadi S, et al. (2014). Superparamagnetic iron oxide nanoparticles for delivery of therapeutic agents: opportunities and challenges. Expert Opin Drug Deliv 11:1449–70.
   PubMed Web of Science ®Google Scholar
• Li C, Wang Y, Zhang X, et al. (2013). Tumor-targeted liposomal drug delivery mediated by a diseleno bond-stabilized cyclic peptide. Int J Nanomedicine 8:1051–62.
   PubMed Web of Science ®Google Scholar
• Li W, Peng J, Tan L, et al. (2016). Mild photothermal therapy/photodynamic therapy/chemotherapy of breast cancer by Lyp-1 modified Docetaxel/IR820 Co-loaded micelles. Biomaterials 106:119–33.
   PubMed Web of Science ®Google Scholar
• Li X, Jin Q, Chen T, et al. (2009). LyP-1 ultrasonic microbubbles targeting to cancer cell as tumor bio-acoustics markers or drug carriers: targeting efficiency evaluation in, microfluidic channels. Conf Proc IEEE Eng Med Biol Soc 2009:463–6.
   PubMedGoogle Scholar
• Libby P, Aikawa M. (2002). Stabilization of atherosclerotic plaques: new mechanisms and clinical targets. Nat Med 8:1257–62.
   PubMed Web of Science ®Google Scholar
• Lin PC, Lin S, Wang PC, et al. (2014). Techniques for physicochemical characterization of nanomaterials. Biotechnol Adv 32:711–26.
   PubMed Web of Science ®Google Scholar
• Liu G, Gao J, Ai H, et al. (2013). Applications and potential toxicity of magnetic iron oxide nanoparticles. Small 9:1533–45.
   PubMed Web of Science ®Google Scholar
• Luo G, Yu X, Jin C, et al. (2010). LyP-1-conjugated nanoparticles for targeting drug delivery to lymphatic metastatic tumors. Int J Pharm 385:150–6.
   PubMed Web of Science ®Google Scholar
• Lusic H, Grinstaff MW. (2013). X-ray-computed tomography contrast agents. Chem Rev 113:1641–66.
   PubMed Web of Science ®Google Scholar
• Makela AR, Enback J, Laakkonen JP, et al. (2008). Tumor targeting of baculovirus displaying a lymphatic homing peptide. J Gene Med 10:1019–31.
   PubMed Web of Science ®Google Scholar
• Makela AR, Matilainen H, White DJ, et al. (2006). Enhanced baculovirus-mediated transduction of human cancer cells by tumor-homing peptides. J Virol 80:6603–11.
   PubMed Web of Science ®Google Scholar
• Mallory M, Gogineni E, Jones GC, et al. (2016). Therapeutic hyperthermia: the old, the new, and the upcoming. Crit Rev Oncol Hematol 97:56–64.
   PubMed Web of Science ®Google Scholar
• Martin KH, Dayton PA. (2013). Current status and prospects for microbubbles in ultrasound theranostics. Wiley Interdiscip Rev Nanomed Nanobiotechnol 5:329–45.
   PubMed Web of Science ®Google Scholar
• Matthews DA, Russell WC. (1998). Adenovirus core protein V interacts with p32–a protein which is associated with both the mitochondria and the nucleus. J Gen Virol 79:1677–85.
   PubMed Web of Science ®Google Scholar
• Murakami H, Blobel G, Pain D. (1993). Signal sequence region of mitochondrial precursor proteins binds to mitochondrial import receptor. Proc Natl Acad Sci USA 90:3358–62.
   PubMed Web of Science ®Google Scholar
• Muta T, Kang D, Kitajima S, et al. (1997). p32 protein, a splicing factor 2-associated protein, is localized in mitochondrial matrix and is functionally important in maintaining oxidative phosphorylation. J Biol Chem 272:24363–70.
   PubMed Web of Science ®Google Scholar
• Nehate C, Jain S, Saneja A, et al. (2014). Paclitaxel formulations: challenges and novel delivery options. Curr Drug Deliv 11:666–86.
   PubMed Web of Science ®Google Scholar
• Omidfar K, Daneshpour M. (2015). Advances in phage display technology for drug discovery. Expert Opin Drug Discov 10:651–69.
   PubMed Web of Science ®Google Scholar
• Park JH, von Maltzahn G, Xu MJ, et al. (2010). Cooperative nanomaterial system to sensitize, target, and treat tumors. Proc Natl Acad Sci USA 107:981–6.
   PubMed Web of Science ®Google Scholar
• Peerschke EI, Minta JO, Zhou SZ, et al. (2004). Expression of gC1q-R/p33 and its major ligands in human atherosclerotic lesions. Mol Immunol 41:759–66.
   PubMed Web of Science ®Google Scholar
• Ren Y, Cheung HW, von Maltzhan G, et al. (2012). Targeted tumor-penetrating siRNA nanocomplexes for credentialing the ovarian cancer oncogene ID4. Sci Transl Med 4:147ra12.
   Web of Science ®Google Scholar
• Ren Y, Hauert S, Lo JH, et al. (2012). Identification and characterization of receptor-specific peptides for siRNA delivery. ACS Nano 6:8620–31.
   PubMed Web of Science ®Google Scholar
• Roth L, Agemy L, Kotamraju VR, et al. (2012). Transtumoral targeting enabled by a novel neuropilin-binding peptide. Oncogene 31:3754–63.
   PubMed Web of Science ®Google Scholar
• Seidi K, Neubauer HA, Moriggl R, et al. (2018). Tumor target amplification: implications for nano drug delivery systems. J Control Release 275:142–61.
   PubMed Web of Science ®Google Scholar
• Sengupta A, Tyagi RK, Datta K. (2004). Truncated variants of hyaluronan-binding protein 1 bind hyaluronan and induce identical morphological aberrations in COS-1 cells. Biochem J 380:837–44.
   PubMed Web of Science ®Google Scholar
• Seo JW, Baek H, Mahakian LM, et al. (2014). 64Cu-labeled LyP-1-dendrimer for PET-CT imaging of atherosclerotic plaque. Bioconjug Chem 25:231–9.
   PubMed Web of Science ®Google Scholar
• She ZG, Hamzah J, Kotamraju VR, et al. (2016). Plaque-penetrating peptide inhibits development of hypoxic atherosclerotic plaque. J Control Release 238:212–20.
   PubMed Web of Science ®Google Scholar
• Sleeman JP. (2015). The lymph node pre-metastatic niche. J Mol Med 93:1173–84.
   PubMed Web of Science ®Google Scholar
• Soltys BJ, Kang D, Gupta RS. (2000). Localization of P32 protein (gC1q-R) in mitochondria and at specific extramitochondrial locations in normal tissues. Histochem Cell Biol 114:245–55.
   PubMed Web of Science ®Google Scholar
• Storz P, Hausser A, Link G, et al. (2000). Protein kinase C [micro] is regulated by the multifunctional chaperon protein p32. J Biol Chem 275:24601–7.
   PubMed Web of Science ®Google Scholar
• Su CW, Yen CS, Chiang CS, et al. (2017). Multistage continuous targeting with quantitatively controlled peptides on chitosan-lipid nanoparticles with multicore-shell nanoarchitecture for enhanced orally administrated anticancer in vitro and in vivo. Macromol Biosci 17:1600260.
   Web of Science ®Google Scholar
• Sugahara KN, Teesalu T, Karmali PP, et al. (2009). Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 16:510–20.
   PubMed Web of Science ®Google Scholar
• Sugahara KN, Teesalu T, Karmali PP, et al. (2010). Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 328:1031–5.
   PubMed Web of Science ®Google Scholar
• Teesalu T, Sugahara KN, Kotamraju VR, et al. (2009). C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci USA 106:16157–62.
   PubMed Web of Science ®Google Scholar
• Teo P, Wang X, Zhang J, et al. (2018). LyP-1-conjugated Fe3O4 nanoparticles suppress tumor growth by magnetic induction hyperthermia. J Biomater Sci Polym Ed 29:181–94.
   PubMed Web of Science ®Google Scholar
• Timur SS, Bhattarai P, Gursoy RN, et al. (2017). Design and in vitro evaluation of bispecific complexes and drug conjugates of anticancer peptide, LyP-1 in human breast cancer. Pharm Res 34:352–64.
   PubMed Web of Science ®Google Scholar
• Timur SS, Yalcin G, Cevik O, et al. (2018). Molecular dynamics, thermodynamic, and mutational binding studies for tumor-specific LyP-1 in complex with p32. J Biomol Struct Dyn 36:1134–44.
   PubMed Web of Science ®Google Scholar
• Toraya-Brown S, Fiering S. (2014). Local tumour hyperthermia as immunotherapy for metastatic cancer. Int J Hyperthermia 30:531–9.
   PubMed Web of Science ®Google Scholar
• Uchida M, Kosuge H, Terashima M, et al. (2011). Protein cage nanoparticles bearing the LyP-1 peptide for enhanced imaging of macrophage-rich vascular lesions. ACS Nano 5:2493–502.
   PubMed Web of Science ®Google Scholar
• Viola J, Soehnlein O. (2015). Atherosclerosis - A matter of unresolved inflammation. Semin Immunol 27:184–93.
   PubMed Web of Science ®Google Scholar
• Vlahov IR, Leamon CP. (2012). Engineering folate-drug conjugates to target cancer: from chemistry to clinic. Bioconjug Chem 23:1357–69.
   PubMed Web of Science ®Google Scholar
• von Maltzahn G, Ren Y, Park JH, et al. (2008). In vivo tumor cell targeting with "click" nanoparticles. Bioconjug Chem 19:1570–8.
   PubMed Web of Science ®Google Scholar
• Wahajuddin, Arora S. (2012). Superparamagnetic iron oxide nanoparticles: magnetic nanoplatforms as drug carriers. Int J Nanomedicine 7:3445–71.
   PubMed Web of Science ®Google Scholar
• Wang S, Placzek WJ, Stebbins JL, et al. (2013). Novel targeted system to deliver chemotherapeutic drugs to EphA2-expressing cancer cells. J Med Chem 55:2427–36.
   Web of Science ®Google Scholar
• Wang TW, Yeh CW, Kuan CH, et al. (2017). Tailored design of multifunctional and programmable pH-responsive self-assembling polypeptides as drug delivery nanocarrier for cancer therapy. Acta Biomater 58:54–66.
   PubMed Web of Science ®Google Scholar
• Wang Z, Yu Y, Ma J, et al. (2012). LyP-1 modification to enhance delivery of artemisinin or fluorescent probe loaded polymeric micelles to highly metastatic tumor and its lymphatics. Mol Pharm 9:2646–57.
   PubMed Web of Science ®Google Scholar
• Wilson HM, Barker RN, Erwig LP. (2009). Macrophages: promising targets for the treatment of atherosclerosis. Curr Vasc Pharmacol 7:234–43.
   PubMed Web of Science ®Google Scholar
• Yan F, Li X, Jiang C, et al. (2014). A novel microfluidic chip for assessing dynamic adhesion behavior of cell-targeting microbubbles. Ultrasound Med Biol 40:148–57.
   PubMed Web of Science ®Google Scholar
• Yan F, Li X, Jin Q, et al. (2011). Therapeutic ultrasonic microbubbles carrying paclitaxel and LyP-1 peptide: preparation, characterization and application to ultrasound-assisted chemotherapy in breast cancer cells. Ultrasound Med Biol 37:768–79.
   PubMed Web of Science ®Google Scholar
• Yan Z, Wang F, Wen Z, et al. (2012). LyP-1-conjugated PEGylated liposomes: a carrier system for targeted therapy of lymphatic metastatic tumor. J Control Release 157:118–25.
   PubMed Web of Science ®Google Scholar
• Yan Z, Zhan C, Wen Z, et al. (2011). LyP-1-conjugated doxorubicin-loaded liposomes suppress lymphatic metastasis by inhibiting lymph node metastases and destroying tumor lymphatics. Nanotechnology 22:415103.
   PubMed Web of Science ®Google Scholar
• Yenugonda V, Nomura N, Kouznetsova V, et al. (2017). A novel small molecule inhibitor of p32 mitochondrial protein overexpressed in glioma. J Transl Med 15:210.
   PubMed Web of Science ®Google Scholar
• Yu MM, Wang RF, Chen YH, et al. (2013). Radiolabeling LyP-1 peptide and preliminary biodistribution evaluation in mice bearing MDA-MB-435 xenografts. Chin Med J 126:471–5.
   PubMed Web of Science ®Google Scholar
• Yu X, Li A, Zhao C, et al. (2017). Ultrasmall semimetal nanoparticles of bismuth for dual-modal computed tomography/photoacoustic imaging and synergistic thermoradiotherapy. ACS Nano 11:3990–4001.
   PubMed Web of Science ®Google Scholar
• Zhang F, Niu G, Lin X, et al. (2012). Imaging tumor-induced sentinel lymph node lymphangiogenesis with LyP-1 peptide. Amino Acids 42:2343–51.
   PubMed Web of Science ®Google Scholar
• Zhang X, Wang F, Shen Q, et al. (2018). Structure reconstruction of LyP-1: Lc(LyP-1) coupling by amide bond inspires the brain metastatic tumor targeted drug delivery. Mol Pharm 15:430–6.
   PubMed Web of Science ®Google Scholar