Chowdhury S, Castro S, Coker C,

2022.07.31
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Chowdhury S, Castro S, Coker C,

Chowdhury S, Castro S, Coker C, Hinchliffe TE, Arpaia N, Danino T. Programmable bacteria induce durable tumor regression and systemic antitumor immunity. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). doi: 10.1007/s00259-019-04347-y, 219. Nat Rev Cancer. doi: 10.1016/j.ejca.2012.07.019, 72. (2019) 120:1078795. (2019) 16:314556. Roovers RC, Vosjan MJWD, Laeremans T, El Khoulati R, De Bruin RCG, Ferguson KM, et al. J Clin Oncol. (2013) 165:1108. doi: 10.2967/jnumed.118.224170, 36. 99mTc-EGFR (27), 99mTc-EGFR-cartilage oligomeric matrix protein (COMP) (28), 99mTc-dipeptidyl-peptidase-like protein 6 (DPP6) (29), 99mTc-mesothelin (30), and 131I-HER2 (31) nanobodies nanobody probes have also demonstrated high T/B ratios. Li C, Feng H, Xia X, Wang L, Gao B, Zhang Y, et al. J Exp Clin Cancer Res. De Groeve et al. Modular design of nanobody-drug conjugates for targeted-delivery of platinum anticancer drugs with an MRI contrast agent. Camelid Ig V genes reveal significant human homology not seen in therapeutic target genes, providing for a powerful therapeutic antibody platform. (2019). Use of 18F-2-fluorodeoxyglucose to label antibody fragments for immuno-positron emission tomography of pancreatic cancer. Clin Cancer Res. Rashidian M, Ingram JR, Dougan M, Dongre A, Whang KA, LeGall C, et al. Xie YJ, Dougan M, Jailkhani N, Ingram J, Fang T, Kummer L, et al. Screening and antitumor effect of an anti-CTLA-4 nanobody. Hassani M, Hajari Taheri F, Sharifzadeh Z, Arashkia A, Hadjati J, van Weerden WM, et al. Homayouni et al. Mol Imaging. Nonetheless, immunogenicity could be further minimized through humanization, which is generally accomplished through replacing various surface regions with human sequences. (2014) 3:1136. (2013) 13:93845. Int J Mol Sci. (2018) 12:264554. Sci Transl Med. (2018) 31:26775. J Nucl Med. Additionally, anti-EGFR-nanobody micelles carrying doxorubicin (175, 176) and anti-EGFR-nanobody liposomes carrying kinase inhibitors (177) demonstrated enhanced anti-tumor efficacy in vivo (176, 177). Photo: courtesy of Robert-Owen-Wahl from Pixabay. J Nucl Med. (2014) 5:530419. Notably, programmable bacteria that release CD47-targeting nanobodies in the TME increased tumor regression and metastatic inhibition in vivo (214). J Nucl Med. Some target DC surface proteins such as CD11b (128, 129), CD36 (128), and MHC-II (128, 130), and others have been designed to block ICPs CTLA-4 (131), and PD-L1 (132) to enhance DC-mediated T cell activation. doi: 10.15171/ijb.1427, 84. First-in-human, first-in-class phase I trial of the anti-CD47 antibody Hu5F9-G4 in patients with advanced cancers. You can help Wikipedia by expanding it. (2013) 30:2059. Hepatology. Xie YJ, Dougan M, Ingram JR, Pishesha N, Fang T, Momin N, et al. N Engl J Med. Drug Test Anal. A similar anti-VEGFR2 nanobody conjugated to DOS-47 has been developed for angiogenesis inhibition (169). In vivo near-infrared fluorescence targeting of T cells: Comparison of nanobodies and conventional monoclonal antibodies. (2013) 10:371727. doi: 10.1073/pnas.0505379103, 6. Nanobodies targeting the interaction interface of programmed death receptor 1 (PD-1)/PD-1 ligand 1 (PD-1/PD-L1). J Control Release. Various studies have conjugated nanobodies to TPPs to improve specificity and penetration. doi: 10.1089/hyb.2008.0079. doi: 10.1016/j.bbrc.2019.08.160, 80. Multifunctional transmembrane protein ligands for cell-specific targeting of plasma membrane-derived vesicles. Cancer Immunol Res. Kwon S, Duarte JN, Li Z, Ling JJ, Cheneval O, Durek T, et al. Wang C, Gao W, Feng M, Pastan I, Ho M. Construction of an immunotoxin, HN3-mPE24, targeting glypican-3 for liver cancer therapy. Development of VEGFR2-specific nanobody pseudomonas exotoxin a conjugated to provide efficient inhibition of tumor cell growth. doi: 10.1080/10826068.2019.1692217, 81. (2014) 35:60110. Tian B, Wong WY, Uger MD, Wisniewski P, Chao H. National Research Council of Canada (NRC)Development and characterization of a camelid single domain antibody urease conjugate that targets vascular endothelial growth factor receptor 2.

Furthermore, nanobodies targeting delta-like ligand 4 (DLL4) (92) and CD3 (93) have demonstrated inhibition of neovascularization and tumor proliferation in vitro (92) and in vivo (93). (2013) 87:113048. Polymer-based NPs (181) composed of albumin (182, 183), and polyethyleneimine-PEG (184) demonstrated tumor proliferation inhibition. Mol Imaging Biol. Identification of nanobodies against the acute myeloid leukemia marker cd33. Cancer Biol Ther. J Biomed Nanotechnol. A novel CD7 chimeric antigen receptor-modified NK-92MI cell line targeting T-cell acute lymphoblastic leukemia. doi: 10.1016/j.bbrc.2014.02.069, 89. (2019) 47:50111. Artif Cells Nanomed Biotechnol. doi: 10.1016/S0022-2836(02)01237-8, 3. Another study revealed the myeloid compartment's role in PD-1 blockade response using PEGylated 89Zr-CD8+and 89Zr-CD11b+ nanobodies (44). The S-Fab was PEGylated to extend its serum half-life and reported uncompromised anti-tumor activity (97). Tintelnot J, Baum N, Schulthei C, Braig F, Trentmann M, Finter J, et al. Structural basis of a novel PD-L1 nanobody for immune checkpoint blockade. Schoonaert L, Ru L, Roucourt B, Timmers M, Little S, Chvez-Gutirrez L, et al. Zhao C, Busch DJ, Vershel CP, Stachowiak JC. (2018) 9:4809. doi: 10.1038/s41467-018-07195-w, 103. Vosjan MJWD, Vercammen J, Kolkman JA, Stigter-Van Walsum M, Revets H, Van Dongen GAMS. Small. EY and KS: literature review and interpretation, manuscript writing, and final approval of manuscript. Additionally, unlike mAbs, nanobodies lack an Fc region, and thus cannot directly initiate an Fc-mediated immune response. This review highlights how nanobodies have enhanced various cancer diagnostic tools and therapies, both alone, and synergistically. In light of these various applications, their greatest potential may be found in intracellular targeting. doi: 10.2174/1871527317666181114134518, 148. Montemagno C, Cassim S, Trichanh D, Savary C, Pouyssegur J, Pags G, et al. (2017) 15:7886. Neoleukin is a biopharmaceutical company creating next generation immunotherapies using de novo protein design technology. Wen B, Zhao L, Wang Y, Qiu C, Xu Z, Huang K, et al. Dougan M, Ingram JR, Jeong HJ, Mosaheb MM, Bruck PT, Ali L, et al.

Cell Mol Life Sci. Neoleukin uses sophisticated computational methods to design proteins that demonstrate specific pharmaceutical properties that provide potentially superior therapeutic benefit over native proteins. In addition to intrinsically therapeutic behavior, nanobodies can be utilized to augment the efficacy of other cancer therapies, especially in targeting the TME (Figure 2). Albert S, Arndt C, Feldmann A, Bergmann R, Bachmann D, Koristka S, et al. doi: 10.4161/19420862.2014.975099, 63. (2012) 109:166427. (2007) 56:30317. Proc Natl Acad Sci USA. (2019) 37:94653. Anti-HER2 nanobodies conjugated to branched gold NPs could remove HER2+ cells upon 5 min of laser treatment (202), and anti-EGFR (203205), anti-c-Met (205), and anti-U28 (206) nanobody-PS conjugates demonstrated targeted phototoxicity in vitro (203, 205, 206), and in vivo (203). doi: 10.1158/1535-7163.MCT-18-0849, 57. Additionally, intrabodies developed against B-cell receptor-associated protein 31 (BAP31), have demonstrated caspase-dependent tumor apoptosis in vivo (213). Novel CD7-specific nanobody-based immunotoxins potently enhanced apoptosis of CD7-positive malignant cells. Artif Cells Nanomed Biotechnol. Mol Imaging Biol. Mol Cancer Ther. (2019) 71:1696711. (2012) 8:51625. Behdani M, Zeinali S, Khanahmad H, Karimipour M, Asadzadeh N, Azadmanesh K, et al. Suzuki T, Yamaguchi H, Ogura J, Kobayashi M, Yamada T, Iseki K. Megalin contributes to kidney accumulation and nephrotoxicity of colistin. Tian B, Wong WY, Hegmann E, Gaspar K, Kumar P, Chao H. Production and characterization of a camelid single domain antibody-urease enzyme conjugate for the treatment of cancer. (2016) 55:241620. doi: 10.1093/protein/gzw043, 147. Their robustness and manufacturing ease are favorable for large-scale production, and their superior paratope diversity allows an extensive arsenal for tumor antigen targeting. Khaleghi S, Rahbarizadeh F, Ahmadvand D, Hosseini HRM. Small. 105. Heukers R, Fan TS, de Wit RH, van Senten JR, De Groof TWM, Bebelman MP, et al. (2014) 446:1326. (2010) 145:16575. (39) study suggest that an Fc domain may be needed for clinically-relevant potency. The balance between anti-tumor and pro-tumor macrophages is another critical component that dictates the TME; thus, their targeting would be useful in illuminating overall macrophage polarization. L-DOS47 is a recently developed nanobody-urease enzyme conjugate targeting CEACAM6 (168) and is currently in phase I/II clinical trials. doi: 10.1021/acs.molpharmaceut.8b00584, 107. Similarly, bispecific light T-cell engagers (LiTEs) targeting EGFR and CD3 have demonstrated T cell-mediated tumor lysis with minimal cytotoxicity (100). Open Biol. Ultrasound imaging utilizes reflected sound waves from tissues, and nanobodies have been tagged to contrast agents, microbubbles, and nanobubbles. Anti-CTLA-4 therapy requires an Fc domain for efficacy. doi: 10.1016/j.pep.2019.02.003, 55. Pruszynski M, D'Huyvetter M, Bruchertseifer F, Morgenstern A, Lahoutte T. Evaluation of an anti-her2 nanobody labeled with 225 ac for targeted -particle therapy of cancer. (2019)20:4818. doi: 10.3390/ijms20194818, 64. doi: 10.1021/acs.molpharmaceut.9b00360, 207. doi: 10.1038/srep03571, 112. (2019) 29:83245. Table 3. Early phase I study of a 99mTc-labeled anti-programmed death ligand-1 (PD-L1) single-domain antibody in SPECT/CT assessment of PD-L1 expression in non-small cell lung cancer. doi: 10.1021/nn1023363, 203. However, their short half-lives are incompatible with the large size, and slow tissue clearance of mAbs; thus, nanobodies hold potential as improved delivery vectors. Huang H, Wu T, Shi H, Wu Y, Yang H, Zhong K, et al. Nanomed Nanotechnol Biol Med. (2015) 1:1427. Oncotarget. (2013) 57:631924. doi: 10.1007/978-1-4757-1445-6_2, 47. doi: 10.1002/jcb.29111, 56. Repeatability of 68-GaNOTA-Anti-HER2 VHH1 PET/CT in Breast Carcinoma Patients (VUBAR). Hassani M, Hajari Taheri F, Sharifzadeh Z, Arashkia A, Hadjati J, van Weerden WM, et al. Mol Biotechnol. (2017) 9:30297305. doi: 10.3892/ol.2019.10320, 19. Molecular imaging utilizes a molecular probe that binds to a tumor antigen. Hybridoma. Noninvasive imaging of the immune checkpoint LAG-3 using nanobodies, from development to pre-clinical use. (2019) 25:105763. J Control Release. Mol Cancer Ther. Li S, Zhang W, Jiang K, Shan H, Shi M, Chen B, et al. The structural basis of nanobody unfolding reversibility and thermoresistance. Despite the preclinical success of cytokine-based therapy, clinical studies have been met with subpar efficacy due to their narrow therapeutic window and short half-life. Durable antitumor responses to CD47 blockade require adaptive immune stimulation. (45) developed a novel anti-EIIIB nanobody (splice variant of fibronectin) that enhanced detection of tumors, metastasis, and fibroses. Wang Y, Wang Y, Chen G, Li Y, Xu W, Gong S. Quantum-dot-based theranostic micelles conjugated with an anti-EGFR NANOBODY FOR TRIPLE-NEGATIVE BREAST CANCER THERAPY. MAbs. PLoS ONE. Cancers. Bioconjug Chem. Viral vectors have also shown potential for targeting tumor vasculature, and Ahani et al. Currently, antibodies targeting the molecules PD-1/PD-L1 and CTLA-4 have been FDA approved (76); however, their potency remains inconsistent, with minimal efficacy in most patients. Bakhtiari SHA, Rahbarizadeh F, Hasannia S, Ahmadvand D, Iri-Sofla FJ, Rasaee MJ. doi: 10.1093/protein/gzy017, 7. (2019) 21:898906. Anti-HER2 VHH targeted magnetoliposome for intelligent magnetic resonance imaging of breast cancer cells. doi: 10.1016/j.molimm.2019.12.017, 100. Biotechnol Lett. Much of the focus in cancer is placed on therapeutics, but the diagnostics of tumor imaging are just as critical, as visual knowledge of the tumor's antigen profile is needed to maximize therapeutic efficacy. Utilizing the penetration capacity and structural simplicity of nanobodies, studies have explored the implementation of nanobody-based antigen conjugates to enhance DC-based immunity. doi: 10.1080/2162402X.2017.1377874, 102. Active targeting of dendritic polyglycerols for diagnostic cancer imaging. Neoleukins lead product candidate. (2016) 291:1264157. Other explored implementations are nanobody-conjugated extracellular vesicles (186, 187), dendrimers (188), DNA nanoplatforms (189), and nanogels (190), but further studies are needed to characterize these modalities. Protein Eng Des Sel. Targeted delivery of cyclotides via conjugation to a nanobody. Proc Natl Acad Sci USA. Nano Lett. Godar M, Morello V, Sadi A, Hultberg A, De Jonge N, Basilico C, et al.

(2018) 15:457788. Kwon et al. In the context of nanobodies, a BiTE targeting the EGFR and V9V2 TCR stimulated T-cell mediated cytotoxicity against EGFR+ tumor cells in vivo (118).

J Cell Biochem. Mol Pharm. J Control Release. Bispecific light T-cell engagers for gene-based immunotherapy of epidermal growth factor receptor (EGFR)-positive malignancies. J Control Release. Van De Water JAJM, Bagci-Onder T, Agarwal AS, Wakimoto H, Roovers RC, Zhu Y, et al. Generation and characterization of a functional nanobody against inflammatory chemokine CXCL10, as a novel strategy for the treatment of multiple sclerosis. Nanobody-albumin nanoparticles (NANAPs) for the delivery of a multikinase inhibitor 17864 to EGFR overexpressing tumor cells. Predicting the response to CTLA-4 blockade by longitudinal noninvasive monitoring of CD8 T cells. (2018) 67:125160. (2019) 157:5762. Wang H, Wang Y, Xiao Z, Li W, Dimitrov D, Chen W. Human domain antibodies to conserved epitopes on her2 potently inhibit growth of HER2-overexpressing human breast cancer cells in vitro. Immuno-PET identifies the myeloid compartment as a key contributor to the outcome of the antitumor response under PD-1 blockade. Fang T, Duarte JN, Ling J, Li Z, Guzman JS, Hidde P, et al. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hammers C, Songa EB, et al. Nanobodies have spurred the development of commercial companies and have been used in applications such as biosensing, affinity-capture, and protein crystallization; however, their most significant potential lies in therapeutics, especially for cancer. Neutralization of human interleukin 23 by multivalent nanobodies explained by the structure of cytokinenanobody complex. Phase i study of 68Ga-HER2-Nanobody for PET/CT assessment of HER2 expression in breast carcinoma. Mol Immunol. Int J Mol Sci. PET imaging of macrophage mannose receptor-expressing macrophages in tumor stroma using 18F-radiolabeled camelid single-domain antibody fragments. Various studies have demonstrated the efficacy of utilizing MUC-1 (104), CD7 (105), CD38 (106), VEGFR2 (107), prostate-specific membrane antigen (PSMA) (108, 109), glypican-2 (GPC2) (110), and T cell receptor (TCR)-like nanobody-CARs (111) in various tumor models. It is also a comparatively safer technique, but its applications are currently limited to systemic vasculature (12). Peyrassol X, Laeremans T, Gouwy M, Lahura V, Debulpaep M, Van Damme J, et al. Report Locked. Antibodies. (2012) 158:34653. Cancer immunotherapy with T cells carrying bispecific receptors that mimic antibodies. doi: 10.1016/j.canlet.2016.10.031, 144. (2005) 24:50119. Construction of a chimeric antigen receptor bearing a nanobody against prostate a specific membrane antigen in prostate cancer. Adeno-associated viruses (AAVs), adenoviruses (Ads), and lentiviruses (LVs) have been explored; however, their main limitation is their broad tropism (134). As evidenced by existing preclinical studies, the targeting of critical intracellular tumor antigens may be the next pivotal step to revolutionizing a new wave of cancer therapeutics. Deng C, Xiong J, Gu X, Chen X, Wu S, Wang Z, et al. (2013) 122:70514. Yu Y, Li J, Zhu X, Tang X, Bao Y, Sun X, et al. (2019) 18:1418. A novel multifunctional anti-CEA-IL15 molecule displays potent antitumor activities. (2019) 58:142248. Biomaterials. Steels et al. Arbabi-Ghahroudi M, Tanha J, MacKenzie R. Prokaryotic expression of antibodies. Cancers. Broos K, Lecocq Q, De Keersmaecker B, Raes G, Corthals J, Lion E, et al. [1] It is a de novo protein that was first computationally designed at the Institute of Protein Design (IPD), University of Washington. Monovalent and bivalent nanobodies blocked VEGF ligand binding (88, 89) while also inhibiting VEGF-activated proliferation in vivo (89). *Correspondence: Khalid Shah, kshah@bwh.harvard.edu, Nanobodies: Types, Structure, and Mechanism of Action, Nanobodies: Synergy With Other Cancer Therapeutics, https://clinicaltrials.gov/ct2/show/NCT03924466, Creative Commons Attribution License (CC BY). Proc Natl Acad Sci USA. (2019) 8:26. doi: 10.3390/antib8020026, 206. Human epidermal growth factor receptor 3-specific tumor uptake and bioDistribution of 89Zr-MSB0010853 visualized by real-time and noninvasive pet imaging. 99mTc-labeled tetramer and pentamer of single-domain antibody for targeting epidermal growth factor receptor in xenografted tumors. 20. Blood. Goyvaerts C, De Vlaeminck Y, Escors D, Lienenklaus S, Keyaerts M, Raes G, et al. Int J Nanomed. Intrinsically active nanobody-modified polymeric micelles for tumor-targeted combination therapy. An N, Hou YN, Zhang QX, Li T, Zhang QL, Fang C, et al. Hauck B, Xiao W. Characterization of tissue tropism determinants of adeno-associated virus type 1. Bispecific nanobody-CARs targeting CD20 and HER2 have also been developed; however, experiments have yet to be performed in vivo (112). Smolarek D, Hattab C, Hassanzadeh-Ghassabeh G, Cochet S, Gutirrez C, De Brevern AG, et al. Liu Y, Wang Y, Xing J, Li Y, Liu J, Wang Z. Proteasome activator complex PA28 identified as an accessible target in prostate cancer by in vivo selection of human antibodies.