Reviews
Canyu Yang, Bing He, Wenbing Dai, Hua Zhang, Ying Zheng, Xueqing Wang, Qiang Zhang. The role of caveolin-1 in the biofate and efficacy of anti-tumor drugs and their nano-drug delivery systems[J]. Acta Pharmaceutica Sinica B, 2021, 11(4): 961-977

The role of caveolin-1 in the biofate and efficacy of anti-tumor drugs and their nano-drug delivery systems
Canyu Yanga, Bing Heb,d, Wenbing Daib, Hua Zhangb, Ying Zhengc, Xueqing Wanga,b, Qiang Zhanga,b,d
a Department of Pharmacy Administration and Clinical Pharmacy, School of Pharmaceutical Science, Peking University, Beijing 100191, China;
b Beijing Key Laboratory of Molecular Pharmaceutics, New Drug Delivery Systems, School of Pharmaceutical Sciences, Peking University, Beijing 100191, China;
c State Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of Macau, Macau 999078, China;
d State Key Laboratory of Natural and Biomimetic Drugs, Peking University, Beijing 100191, China
Abstract:
As one of the most important components of caveolae, caveolin-1 is involved in caveolaemediated endocytosis and transcytosis pathways, and also plays a role in regulating the cell membrane cholesterol homeostasis and mediating signal transduction. In recent years, the relationship between the expression level of caveolin-1 in the tumor microenvironment and the prognostic effect of tumor treatment and drug treatment resistance has also been widely explored. In addition, the interplay between caveolin-1 and nano-drugs is bidirectional. Caveolin-1 could determine the intracellular biofate of specific nano-drugs, preventing from lysosomal degradation, and facilitate them penetrate into deeper site of tumors by transcytosis; while some nanocarriers could also affect caveolin-1 levels in tumor cells, thereby changing certain biophysical function of cells. This article reviews the role of caveolin-1 in tumor prognosis, chemotherapeutic drug resistance, antibody drug sensitivity, and nano-drug delivery, providing a reference for the further application of caveolin-1 in nano-drug delivery systems.
Key words:    Caveolin-1    Cancer    Drug resistance    Transcytosis    Nano-drug delivery systems    Biofate   
Received: 2020-06-09     Revised: 2020-07-24
DOI: 10.1016/j.apsb.2020.11.020
Funds: This work was supported by the National Natural Science Foundation of China (81872809, 81690264 and 31671017); and the National Key Research and Development Program of China (2017YFA0205600).
Corresponding author: Xueqing Wang, wangxq@bjmu.edu.cn;Qiang Zhang, zqdodo@bjmu.edu.cn     Email:wangxq@bjmu.edu.cn;zqdodo@bjmu.edu.cn
Author description:
Service
PDF(KB) Free
Print
0
Authors
Canyu Yang
Bing He
Wenbing Dai
Hua Zhang
Ying Zheng
Xueqing Wang
Qiang Zhang

References:
1. Sotgia F, Martinez Outschoorn UE, Howell A, Pestell RG, Pavlides S, Lisanti MP. Caveolin-1 and cancer metabolism in the tumor microenvironment:markers, models, and mechanisms. Annu Rev Pathol:Mechanisms of Disease 2012;7:423-67.
2. Cheng JP, Nichols BJ. Caveolae:one function or many?. Trends Cell Biol 2016;26:177-89.
3. Li XA, Everson WV, Smart EJ. Caveolae, lipid rafts, and vascular disease. Trends Cardiovasc Med 2005;15:92-6.
4. Galbiati F, Volonte D, Liu J, Capozza F, Frank PG, Zhu L, et al. Caveolin-1 expression negatively regulates cell cycle progression by inducing G0/G1 arrest via a p53/p21WAF1/Cip1-dependent mechanism. Mol Biol Cell 2001;12:2229-44.
5. Engelman JA, Wykoff CC, Yasuhara S, Song KS, Okamoto T, Lisanti MP. Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 1997;272:16374-81.
6. Torres VA, Tapia JC, Rodríguez DA, Párraga M, Lisboa P, Montoya M, et al. Caveolin-1 controls cell proliferation and cell death by suppressing expression of the inhibitor of apoptosis protein survivin. J Cell Sci 2006;119:1812-23.
7. Xu L, Qu XJ, Li HM, Li C, Liu J, Zheng HC, et al. Src/caveolin-1-regulated EGFR activation antagonizes TRAIL-induced apoptosis in gastric cancer cells. Oncol Rep 2014;32:318-24.
8. Meyer C, Liu Y, Kaul A, Peipe I, Dooley S. Caveolin-1 abrogates TGF-β mediated hepatocyte apoptosis. Cell Death Dis 2013;4. e466-e66.
9. Burgermeister E, Liscovitch M, Röcken C, Schmid RM, Ebert MP. Caveats of caveolin-1 in cancer progression. Cancer Lett 2008;268:187-201.
10. Lamaze C, Prior I. Endocytosis and signaling. New York:Springer; 2018.
11. Gupta R, Toufaily C, Annabi B. Caveolin and cavin family members:dual roles in cancer. Biochimie 2014;107:188-202.
12. Fielding PE, Fielding CJ. Intracellular transport of low density lipoprotein derived free cholesterol begins at clathrin-coated pits and terminates at cell surface caveolae. Biochemistry 1996;35:14932-8.
13. Hayer A, Stoeber M, Ritz D, Engel S, Meyer HH, Helenius A. Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J Cell Biol 2010;191:615-29.
14. Muley H, Fadó R, Rodríguez Rodríguez R, Casals N. Drug uptakebased chemoresistance in breast cancer treatment. Biochem Pharmacol 2020;177:1139-59.
15. Echarri A, Del Pozo MA. Caveolae-mechanosensitive membrane invaginations linked to actin filaments. J Cell Sci 2015;128:2747-58.
16. Anderson RG. The caveolae membrane system. USA:Annual Reviews; 1998. 4139 El Camino Way, PO Box 10139, Palo Alto, CA 94303-0139.
17. Zhou Q, Dong CY, Fan WF, Jiang HP, Xiang JJ, Qiu NS, et al. Tumor extravasation and infiltration as barriers of nanomedicine for high efficacy:the current status and transcytosis strategy. Biomaterials 2020;240:1199-202.
18. Liu Y, Huo YY, Yao L, Xu YW, Meng FQ, Li HF, et al. Transcytosis of nanomedicine for tumor penetration. Nano Lett 2019;19:8010-20.
19. Wu DJ, Zhuo LY, Wang XD. Metabolic reprogramming of carcinomaassociated fibroblasts and its impact on metabolic heterogeneity of tumors. Semin Cell Dev Biol 2017;64:125-31.
20. Martinez Outschoorn UE, Pavlides S, Whitaker Menezes D, Daumer KM, Milliman JN, Chiavarina B, et al. Tumor cells induce the cancer associated fibroblast phenotype via caveolin-1 degradation:implications for breast cancer and DCIS therapy with autophagy inhibitors. Cell Cycle 2010;9:2423-33.
21. Chen DL, Che GW. Value of caveolin-1 in cancer progression and prognosis:emphasis on cancer-associated fibroblasts, human cancer cells and mechanism of caveolin-1 expression. Oncol Lett 2014;8:1409-21.
22. Avagliano A, Granato G, Ruocco MR, Romano V, Belviso I, Carfora A, et al. Metabolic reprogramming of cancer associated fibroblasts:the slavery of stromal fibroblasts. BioMed Res Int 2018. Available from:https://doi/10.1155/2018/6075403.
23. Xing YZ, Zhao SM, Zhou BH, Mi J. Metabolic reprogramming of the tumour microenvironment. FEBS J 2015;282:3892-8.
24. Penkert J, Ripperger T, Schieck M, Schlegelberger B, Steinemann D, Illig T. On metabolic reprogramming and tumor biology:a comprehensive survey of metabolism in breast cancer. Oncotarget 2016;7:67626.
25. Wilde L, Roche M, Domingo Vidal M, Tanson K, Philp N, Curry J, et al. Metabolic coupling and the Reverse Warburg Effect in cancer:implications for novel biomarker and anticancer agent development. Semin Oncol 2017;44:198-203.
26. Witkiewicz AK, Casimiro MC, Dasgupta A, Mercier I, Wang C, Bonuccelli G, et al. Towards a new "stromal-based" classification system for human breast cancer prognosis and therapy. Cell Cycle 2009;8:1654-8.
27. Mercier I, Casimiro MC, Wang C, Rosenberg AL, Quong J, Minkeu A, et al. Human breast cancer-associated fibroblasts (CAFs) show caveolin-1 down-regulation and RB tumor suppressor functional inactivation:implications for the response to hormonal therapy. Cancer Biol Ther 2008;7:1212-25.
28. Sloan EK, Ciocca DR, Pouliot N, Natoli A, Restall C, Henderson MA, et al. Stromal cell expression of caveolin-1 predicts outcome in breast cancer. Am J Pathol 2009;174:2035-43.
29. Witkiewicz AK, Dasgupta A, Sammons S, Er O, Potoczek M, Guiles F, et al. Loss of stromal caveolin-1 expression predicts poor clinical outcome in triple negative and basal-like breast cancers. Cancer Biol Ther 2010;10:135-43.
30. Zhao XD, He YY, Gao J, Fan LF, Li ZH, Yang GF, et al. Caveolin-1 expression level in cancer associated fibroblasts predicts outcome in gastric cancer. PLoS One 2013;8:e59102.
31. Wu KN, Queenan M, Brody JR, Potoczek M, Sotgia F, Lisanti MP, et al. Loss of stromal caveolin-1 expression in malignant melanoma metastases predicts poor survival. Cell Cycle 2011;10:4250-5.
32. Ayala G, Morello M, Frolov A, You S, Li R, Rosati F, et al. Loss of caveolin-1 in prostate cancer stroma correlates with reduced relapsedfree survival and is functionally relevant to tumour progression. J Pathol 2013;231:77-87.
33. Di Vizio D, Morello M, Sotgia F, Pestell RG, Freeman MR, Lisanti MP. An absence of stromal caveolin-1 is associated with advanced prostate cancer, metastatic disease spread and epithelial Akt activation. Cell Cycle 2009;8:2420-4.
34. Park J, Bae E, Lee C, Yoon SS, Chae YS, Ahn KS, et al. RNA interference-directed caveolin-1 knockdown sensitizes SN12CPM6 cells to doxorubicin-induced apoptosis and reduces lung metastasis. Tumor Biol 2010;31:643-50.
35. Parat MO, Riggins GJ. Caveolin-1, caveolae, and glioblastoma. Neuro Oncol 2012;14:679-88.
36. Hulit J, Bash T, Fu M, Galbiati F, Albanese C, Sage DR, et al. The cyclin D1 gene is transcriptionally repressed by caveolin-1. J Biol Chem 2000;275:21203-9.
37. Fiucci G, Ravid D, Reich R, Liscovitch M. Caveolin-1 inhibits anchorage-independent growth, anoikis and invasiveness in MCF-7 human breast cancer cells. Oncogene 2002;21:2365-75.
38. Sunaga N, Miyajima K, Suzuki M, Sato M, White MA, Ramirez RD, et al. Different roles for caveolin-1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res 2004;64:4277-85.
39. Cui J, Rohr LR, Swanson G, Speights VO, Maxwell T, Brothma AR. Hypermethylation of the caveolin-1 gene promoter in prostate cancer. Prostate 2001;46:249-56.
40. Li L, Ren C, Yang G, Goltsov AA, Tabata K, Thompson TC. Caveolin-1 promotes autoregulatory, Akt-mediated induction of cancerpromoting growth factors in prostate cancer cells. Mol Cancer Res 2009;7:1781-91.
41. Mathieu R, Klatte T, Lucca I, Mbeutcha A, Seitz C, Karakiewicz PI, et al. Prognostic value of Caveolin-1 in patients treated with radical prostatectomy:a multicentric validation study. BJU Int 2016;118:243-9.
42. Lee H, Volonte D, Galbiati F, Iyengar P, Lublin DM, Bregman DB, et al. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo:identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol Endocrinol 2000;14:1750-75.
43. Tahir SA, Yang G, Ebara S, Timme TL, Satoh T, Li L, et al. Secreted caveolin-1 stimulates cell survival/clonal growth and contributes to metastasis in androgen-insensitive prostate cancer. Cancer Res 2001; 61:3882-5.
44. Bonuccelli G, Casimiro MC, Sotgia F, Wang C, Liu M, Katiyar S, et al. Caveolin-1 (P132L), a common breast cancer mutation, confers mammary cell invasiveness and defines a novel stem cell/metastasisassociated gene signature. Am J Pathol 2009;174:1650-62.
45. Li ZY, Wang N, Huang CX, Bao YH, Jiang YQ, Zhu GT. Downregulation of caveolin-1 increases the sensitivity of drug-resistant colorectal cancer HCT116 cells to 5-fluorouracil. Oncol Lett 2017; 13:483-7.
46. Zou W, Ma XD, Hua W, Chen BL, Cai GQ. Caveolin-1 mediates chemoresistance in cisplatin-resistant ovarian cancer cells by targeting apoptosis through the Notch-1/Akt/NF-kB pathway. Oncol Rep 2015; 34:3256-63.
47. Yang CPH, Galbiati F, Volonté D, Horwitz SB, Lisanti MP. Upregulation of caveolin-1 and caveolae organelles in Taxol-resistant A549 cells. FEBS Lett 1998;439:368-72.
48. Sung M, Tan X, Lu B, Golas J, Hosselet C, Wang F, et al. Caveolae-mediated endocytosis as a novel mechanism of resistance to trastuzumab emtansine (T-DM1). Mol Cancer Therapeut 2018;17:243-53.
49. Wang X, Lu B, Dai CY, Fu YF, Hao K, Zhao B, et al. Caveolin-1 promotes chemoresistance of gastric cancer cells to cisplatin by activating WNT/b-catenin pathway. Front Oncol 2020;10:46.
50. Liu Y, Fu YL, Hu XX, Chen S, Miao JB, Wang Y, et al. Caveolin-1 knockdown increases the therapeutic sensitivity of lung cancer to cisplatin-induced apoptosis by repressing Parkin-related mitophagy and activating the ROCK1 pathway. J Cell Physiol 2020;235:1197-208.
51. Nagy P, Vereb G, Sebestyén Z, Horváth G, Lockett SJ, Damjanovich S, et al. Lipid rafts and the local density of ErbB proteins influence the biological role of homo-and heteroassociations of ErbB2. J Cell Sci 2002;115:4251-62.
52. Steven S. Overview of the trastuzumab (Herceptin) anti-HER2 monoclonal antibody clinical program in HER2-overexpressing metastatic breast cancer. Herceptin multinational investigator study group. Semin Oncol 1999;4:71-7.
53. Nahta R, Esteva FJ. Herceptin:mechanisms of action and resistance. Cancer Lett 2006;232:123-38.
54. Pereira PM, Sharma SK, Carter LM, Edwards KJ, Pourat J, Ragupathi A, et al. Caveolin-1 mediates cellular distribution of HER2 and affects trastuzumab binding and therapeutic efficacy. Nat Commun 2018;9:5137.
55. Sekhar SC, Kasai T, Satoh A, Shigehiro T, Mizutani A, Murakami H, et al. Identification of caveolin-1 as a potential causative factor in the generation of trastuzumab resistance in breast cancer cells. J Cancer 2013;4:391-401.
56. Ritchie M, Tchistiakova L, Scott N. Implications of receptor-mediated endocytosis and intracellular trafficking dynamics in the development of antibody drug conjugates. mAbs 2013;5:13-21.
57. Barok M, Joensuu H, Isola J. Trastuzumab emtansine:mechanisms of action and drug resistance. Breast Cancer Res 2014;16:209-21.
58. Chung YC, Kuo JF, Wei WC, Chang KJ, Chao WT. Caveolin-1 dependent endocytosis enhances the chemosensitivity of HER-2 positive breast cancer cells to trastuzumab emtansine (T-DM1). PLoS One 2015;10:e0133072.
59. Chung YC, Chang CM, Wei WC, Chang TW, Chang KJ, Chao WT. Metformin-induced caveolin-1 expression promotes T-DM1 drug efficacy in breast cancer cells. Sci Rep 2018;8:3930.
60. Sahay G, Alakhova DY, Kabanov AV. Endocytosis of nanomedicines. J Control Release 2010;145:182-95.
61. Le Roy C, Wrana JL. Clathrin-and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005; 6:112-26.
62. Luo D, Saltzman WM. Synthetic DNA delivery systems. Nat Biotechnol 2000;18:33-7.
63. Fujimoto T, Kogo H, Nomura R, Une T. Isoforms of caveolin-1 and caveolar structure. J Cell Sci 2000;113 Pt 19:3509-17.
64. Sahay G, Kim JO, Kabanov AV, Bronich TK. The exploitation of differential endocytic pathways in normal and tumor cells in the selective targeting of nanoparticulate chemotherapeutic agents. Biomaterials 2010;31:923-33.
65. Gabrielson NP, Pack DW. Efficient polyethylenimine-mediated gene delivery proceeds via a caveolar pathway in HeLa cells. J Control Release 2009;136:54-61.
66. Petrelli F, Borgonovo K, Barni S. Targeted delivery for breast cancer therapy:the history of nanoparticle-albumin-bound paclitaxel. Expet Opin Pharmacother 2010;11:1413-32.
67. Lee JJ, Lee SY, Park JH, Kim DD, Cho HJ. Cholesterol-modified poly (lactide-co-glycolide) nanoparticles for tumor-targeted drug delivery. Int J Pharm 2016;509:483-91.
68. Sundaramoorthy P, Ramasamy T, Mishra SK, Jeong KY, Yong CS, Kim JO, et al. Engineering of caveolae-specific self-micellizing anticancer lipid nanoparticles to enhance the chemotherapeutic efficacy of oxaliplatin in colorectal cancer cells. Acta Biomater 2016;42:220-31.
69. Voigt J, Christensen J, Shastri VP. Differential uptake of nanoparticles by endothelial cells through polyelectrolytes with affinity for caveolae. Proc Natl Acad Sci Unit States Am 2014;111:2942-7.
70. Desai N, Trieu V, Yao Z, Louie L, Ci S, Yang A, et al. Increased antitumor activity, intratumor paclitaxel concentrations, and endothelial cell transport of cremophor-free, albumin-bound paclitaxel, ABI-007, compared with cremophor-based paclitaxel. Clin Cancer Res 2006;12:1317-24.
71. Schettini F, Giuliano M, De Placido S, Arpino G. Nab-paclitaxel for the treatment of triple-negative breast cancer:rationale, clinical data and future perspectives. Cancer Treat Rev 2016;50:129-41.
72. Hawkins MJ, SoonShiong P, Desai N. Protein nanoparticles as drug carriers in clinical medicine. Adv Drug Deliv Rev 2008;60:876-85.
73. Komarova Y, Malik AB. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 2010;72:463-93.
74. Predescu SA, Predescu DN, Malik AB. Molecular determinants of endothelial transcytosis and their role in endothelial permeability. Am J Physiol Lung Cell Mol Physiol 2007;293:L823-42.
75. Wang Z, Tiruppathi C, Minshall RD, Malik AB. Size and dynamics of caveolae studied using nanoparticles in living endothelial cells. ACS Nano 2009;3:4110-6.
76. Nicolì E, Syga MI, Bosetti M, Shastri VP. Enhanced gene silencing through human serum albumin-mediated delivery of polyethylenimine-siRNA polyplexes. PLoS One 2015;10:e0122581.
77. Xu W, Bae EJ, Lee MK. Enhanced anticancer activity and intracellular uptake of paclitaxel-containing solid lipid nanoparticles in multidrugresistant breast cancer cells. Int J Nanomed 2018;13:7549-63.
78. Sakurai Y, Kato A, Harashima H. Involvement of caveolin-1-mediated transcytosis in the intratumoral accumulation of liposomes. Biochem Biophys Res Commun 2020;525:313-8.
79. Zhou Q, Shao SQ, Wang JQ, Xu CH, Xiang JJ, Piao Y, et al. Enzymeactivatable polymer-drug conjugate augments tumour penetration and treatment efficacy. Nat Nanotechnol 2019;14:799-809.
80. Mariam J, Sivakami S, Dongre PM. Albumin corona on nanoparticles-a strategic approach in drug delivery. Drug Deliv 2016;23:2668-76.
81. Chatterjee M, BenJosef E, Robb R, Vedaie M, Seum S, Thirumoorthy K, et al. Caveolae-mediated endocytosis is critical for albumin cellular uptake and response to albumin-bound chemotherapy. Cancer Res 2017;77:5925-37.
82. Borsoi C, Leonard F, Lee Y, Zaid M, Elganainy D, Alexander JF, et al. Gemcitabine enhances the transport of nanovector-albumin-bound paclitaxel in gemcitabine-resistant pancreatic ductal adenocarcinoma. Cancer Lett 2017;403:296-304.
83. Gray SG, Baird AM, O'Kelly F, Nikolaidis G, Almgren M, Meunier A, et al. Gemcitabine reactivates epigenetically silenced genes and functions as a DNA methyltransferase inhibitor. Int J Mol Med 2012;30:1505-11.
84. Zhao YN, Lv FF, Chen S, Wang ZH, Zhang J, Zhang S, et al. Caveolin-1 expression predicts efficacy of weekly Nab-paclitaxel plus gemcitabine for metastatic breast cancer in the phase II clinical trial. BMC Cancer 2018;18:1019.
85. El Gendi SM, Mostafa MF, El Gendi AM. Stromal caveolin-1 expression in breast carcinoma. Correlation with early tumor recurrence and clinical outcome. Pathol Oncol Res 2012;18:459-69.
86. Elsheikh S, Green A, Rakha E, Samaka R, Ammar A, Powe D, et al. Caveolin 1 and caveolin 2 are associated with breast cancer basal-like and triple-negative immunophenotype. Br J Cancer 2008;99:327-34.
87. Witkiewicz AK, Dasgupta A, Sotgia F, Mercier I, Pestell RG, Sabel M, et al. An absence of stromal caveolin-1 expression predicts early tumor recurrence and poor clinical outcome in human breast cancers. Am J Pathol 2009;174:2023-34.
88. Kim TH, Jiang HH, Youn YS, Park CW, Tak KK, Lee S, et al. Preparation and characterization of water-soluble albumin-bound curcumin nanoparticles with improved antitumor activity. Int J Pharm 2011;403:285-91.
89. Zheng Y, Wu J, Shan W, Wu L, Zhou R, Liu M, et al. Multifunctional nanoparticles enable efficient oral delivery of biomacromolecules via improving payload stability and regulating the transcytosis pathway. ACS Appl Mater Interfaces 2018;10:34039-49.
90. Fichter KM, Ingle NP, McLendon PM, Reineke TM. Polymeric nucleic acid vehicles exploit active interorganelle trafficking mechanisms. ACS Nano 2013;7:347-64.
91. Munsell EV, Ross N, O Sullivan M. Journey to the center of the cell:current nanocarrier design strategies targeting biopharmaceuticals to the cytoplasm and nucleus. Curr Pharmaceut Des 2016;22:1227-44.
92. Rejman J, Bragonzi A, Conese M. Role of clathrin-and caveolaemediated endocytosis in gene transfer mediated by lipo-and polyplexes. Mol Ther 2005;12:468-74.
93. Ross NL, Sullivan MO. Overexpression of caveolin-1 in inflammatory breast cancer cells enables IBC-specific gene delivery and prodrug conversion using histone-targeted polyplexes. Biotechnol Bioeng 2016;113:2686-97.
94. Nehoff H, Parayath NN, Taurin S, Greish K. The influence of drug loading on caveolin-1 mediated intracellular internalization of doxorubicin nanomicelles in vitro. J Nanomed Nanotechnol 2014;5:197.
95. Wei X, Wei R, Jiang GY, Jia YJ, Lou H, Yang ZY, et al. Mechanical cues modulate cellular uptake of nanoparticles in cancer via clathrinmediated and caveolae-mediated endocytosis pathways. Nanomedicine 2019;14:613-26.
96. Xiang S, Sarem M, Shah S, Shastri VP. Liposomal treatment of cancer cells modulates uptake pathway of polymeric nanoparticles by altering membrane stiffness. Small 2018;14:17042-5.
97. Dixit S, Sahu R, Verma R, Duncan S, Giambartolomei GH, Singh SR, et al. Caveolin-mediated endocytosis of the Chlamydia M278 outer membrane peptide encapsulated in poly (lactic acid)-poly (ethylene glycol) nanoparticles by mouse primary dendritic cells enhances specific immune effectors mediated by MHC class II and CD4+ T cells. Biomaterials 2018;159:130-45.
Similar articles:
1.Kai Yuan, Xiao Wang, Haojie Dong, Wenjian Min, Haiping Hao, Peng Yang.Selective inhibition of CDK4/6: A safe and effective strategy for developing anticancer drugs[J]. Acta Pharmaceutica Sinica B, 2021,11(1): 30-54
2.Jinghui Zhang, Jiajun Fan, Xian Zeng, Mingming Nie, Jingyun Luan, Yichen Wang, Dianwen Ju, Kai Yin.Hedgehog signaling in gastrointestinal carcinogenesis and the gastrointestinal tumor microenvironment[J]. Acta Pharmaceutica Sinica B, 2021,11(3): 609-620
3.Senling Feng, Huifang Zhou, Deyan Wu, Dechong Zheng, Biao Qu, Ruiming Liu, Chen Zhang, Zhe Li, Ying Xie, Hai-Bin Luo.Nobiletin and its derivatives overcome multidrug resistance (MDR) in cancer: total synthesis and discovery of potent MDR reversal agents[J]. Acta Pharmaceutica Sinica B, 2020,10(2): 327-343
4.Lu Liang, Jijun Fu, Siran Wang, Huiyu Cen, Lingmin Zhang, Safur Rehman Mandukhail, Lingran Du, Qianni Wu, Peiquan Zhang, Xiyong Yu.MiR-142-3p enhances chemosensitivity of breast cancer cells and inhibits autophagy by targeting HMGB1[J]. Acta Pharmaceutica Sinica B, 2020,10(6): 1036-1046
5.Linlin Chang, Yan Hu, Yingying Fu, Tianyi Zhou, Jun You, Jiamin Du, Lin Zheng, Ji Cao, Meidan Ying, Xiaoyang Dai, Dan Su, Qiaojun He, Hong Zhu, Bo Yang.Targeting slug-mediated non-canonical activation of c-Met to overcome chemo-resistance in metastatic ovarian cancer cells[J]. Acta Pharmaceutica Sinica B, 2019,9(3): 484-495
6.Yixian Zhou, Guilan Quan, Qiaoli Wu, Xiaoxu Zhang, Boyi Niu, Biyuan Wu, Ying Huang, Xin Pan, Chuanbin Wu.Mesoporous silica nanoparticles for drug and gene delivery[J]. Acta Pharmaceutica Sinica B, 2018,8(2): 165-177
7.Feifei Liu, Xiaotong Yang, Meiyu Geng, Min Huang.Targeting ERK, an Achilles' Heel of the MAPK pathway, in cancer therapy[J]. Acta Pharmaceutica Sinica B, 2018,8(4): 552-562
8.Xin An, Cesar Sarmiento, Tao Tan, Hua Zhu.Regulation of multidrug resistance by microRNAs in anti-cancer therapy[J]. Acta Pharmaceutica Sinica B, 2017,7(1): 38-51
9.Chongwen Bi, Cheng Ye, Yinghong Li, Wuli Zhao, Rongguang Shao, Danqing Song.Synthesis and biological evaluation of 12-N-p-chlorobenzyl sophoridinol derivatives as a novel family of anticancer agents[J]. Acta Pharmaceutica Sinica B, 2016,6(3): 222-228
Similar articles: