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Application Of Collagen-Model Triple-Helical Peptide-Amphiphiles For CD44-Targeted Drug Delivery Systems

M. Ndinguri, A. Zheleznyak, J. Lauer, C. Anderson, G. Fields
Published 2012 · Medicine

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Cancer treatment by chemotherapy is typically accompanied by deleterious side effects, attributed to the toxic action of chemotherapeutics on proliferating cells from nontumor tissues. The cell surface proteoglycan CD44 has been recognized as a cancer stem cell marker. The present study has examined CD44 targeting as a way to selectively deliver therapeutic agents encapsulated inside colloidal delivery systems. CD44/chondroitin sulfate proteoglycan binds to a triple-helical sequence derived from type IV collagen, α1(IV)1263–1277. We have assembled a peptide-amphiphile (PA) in which α1(IV)1263–1277 was sandwiched between 4 repeats of Gly-Pro-4-hydroxyproline and conjugated to palmitic acid. The PA was incorporated into liposomes composed of DSPG, DSPC, cholesterol, and DSPE-PEG-2000 (1 : 4 : 5 : 0.5). Doxorubicin-(DOX-)loaded liposomes with and without 10% α1(IV)1263–1277 PA were found to exhibit similar stability profiles. Incubation of DOX-loaded targeted liposomes with metastatic melanoma M14#5 and M15#11 cells and BJ fibroblasts resulted in IC50 values of 9.8, 9.3, and >100 μM, respectively. Nontargeted liposomes were considerably less efficacious for M14#5 cells. In the CD44+ B16F10 mouse melanoma model, CD44-targeted liposomes reduced the tumor size to 60% of that of the untreated control, whereas nontargeted liposomes were ineffective. These results suggest that PA targeted liposomes may represent a new class of nanotechnology-based drug delivery systems.
This paper references
10.1021/bc900065r
Peptide targeting of platinum anti-cancer drugs.
M. Ndinguri (2009)
Protein-like molecular architecture: biomaterial applications for inducing cellular receptor binding and signal transduction.
G. Fields (1998)
10.1080/10408360290795574
CD44 in Cancer
D. Naor (2002)
10.1002/(SICI)1097-4636(200004)50:1<75::AID-JBM11>3.0.CO;2-A
Ligand accessibility as means to control cell response to bioactive bilayer membranes.
Y. Dori (2000)
10.1134/S0006297910070023
“Smart” liposomal nanocontainers in biology and medicine
Y. Tarahovsky (2010)
Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes.
A. Gabizon (1994)
10.1016/0005-2736(91)90201-I
Pharmacokinetics of stealth versus conventional liposomes: effect of dose.
T. Allen (1991)
10.1089/oli.2008.0168
Hyaluronic acid-modified DOTAP/DOPE liposomes for the targeted delivery of anti-telomerase siRNA to CD44-expressing lung cancer cells.
S. Taetz (2009)
10.1016/S0169-409X(99)00040-X
Anticancer therapy using glucuronate modified long-circulating liposomes.
Oku (1999)
10.1002/JPS.2600791202
Optimization and upscaling of doxorubicin-containing liposomes for clinical use.
S. Amselem (1990)
10.1074/jbc.M108654200
A Requirement for the CD44 Cytoplasmic Domain for Hyaluronan Binding, Pericellular Matrix Assembly, and Receptor-mediated Endocytosis in COS-7 Cells*
H. Jiang (2002)
CELLTITER-GLO™ LUMINESCENT CELL VIABILITY ASSAY FOR CYTOTOXICITY AND CELL PROLIFERATION STUDIES
Michele Arduengo (2003)
10.1007/978-1-59745-430-8_10
Peptide-mediated targeting of liposomes to tumor cells.
E. Rezler (2007)
10.1038/nsmb1201
Structures of the Cd44–hyaluronan complex provide insight into a fundamental carbohydrate-protein interaction
Suneale Banerji (2007)
10.1016/S0264-410X(99)00198-X
Liposomes as vehicles for the presentation of a synthetic peptide containing an epitope of hepatitis A virus.
M. Garcia (1999)
10.1023/A:1016091314940
Effects of Polyethyleneglycol Chain Length and Phospholipid Acyl Chain Composition on the Interaction of Polyethyleneglycol-phospholipid Conjugates with Phospholipid: Implications in Liposomal Drug Delivery
F. Bedu-Addo (2004)
10.1074/jbc.M111.282046
Comparative Metabolic Flux Profiling of Melanoma Cell Lines
D. Scott (2011)
10.1016/0014-5793(91)80699-4
Influence of the steric barrier activity of amphipathic poly(ethyleneglycol) and ganglioside GM1 on the circulation time of liposomes and on the target binding of immunoliposomes in vivo
A. Mori (1991)
10.1046/J.0022-202X.2004.22205.X
Fibroblast invasive migration into fibronectin/fibrin gels requires a previously uncharacterized dermatan sulfate-CD44 proteoglycan.
R. Clark (2004)
10.1038/nrc3023
CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?
M. Zöller (2011)
10.1073/pnas.0610117104
Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma
M. Prince (2007)
Adapter protein for sitespecific conjugation of payloads for targeted drug delivery
M. V. Backer (2004)
10.1016/S1097-2765(04)00080-2
Structure of the regulatory hyaluronan binding domain in the inflammatory leukocyte homing receptor CD44.
P. Teriete (2004)
10.1016/S0168-3659(03)00201-3
Polymer vesicles in vivo: correlations with PEG molecular weight.
P. Photos (2003)
10.1074/JBC.M003084200
Differences in hyaluronic acid-mediated functions and signaling in arterial, microvessel, and vein-derived human endothelial cells.
V. Lokeshwar (2000)
10.1593/NEO.03460
Tumor-targeted hyaluronan nanoliposomes increase the antitumor activity of liposomal Doxorubicin in syngeneic and human xenograft mouse tumor models.
D. Peer (2004)
10.1021/mp800024g
Anticancer therapeutics: targeting macromolecules and nanocarriers to hyaluronan or CD44, a hyaluronan receptor.
Virginia M Platt (2008)
10.1021/JA981654Z
MINIMAL LIPIDATION STABILIZES PROTEIN-LIKE MOLECULAR ARCHITECTURE
Ying-Ching Yu (1998)
10.1006/EXCR.1996.0384
A chondroitin/dermatan sulfate form of CD44 is a receptor for collagen XIV (undulin).
T. Ehnis (1996)
10.1002/JPS.10062
Targeting of liposomes to melanoma cells with high levels of ICAM-1 expression through adhesive peptides from immunoglobulin domains.
M. R. Jaafari (2002)
10.1016/S0169-409X(99)00037-X
Mechanisms and kinetics of liposome-cell interactions.
Düzgüneş (1999)
CD 44 / Chondroitin Sulfate Proteoglycan and a 2131 Integrin Mediate Human Melanoma Cell Migration on Type IV Collagen and Invasion of Basement Membranes
J. Knutson
10.1016/0005-2736(94)00235-H
Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro.
R. Lee (1995)
10.1021/LA011121V
Stabilization of Phosphatidylserine/Phosphatidylethanolamine Liposomes with Hydrophilic Polymers Having Multiple “Sticky Feet”
Melinda L. Hwang (2001)
Migration of highly aggressive melanoma cells on hyaluronic acid is associated with functional changes, increased turnover and shedding of CD44 receptors.
M. Goebeler (1996)
10.1074/JBC.M212246200
Melanoma Cell CD44 Interaction with the α1(IV)1263–1277 Region from Basement Membrane Collagen Is Modulated by Ligand Glycosylation*
J. Lauer-Fields (2003)
Isolation and identification of cancer stem-like cells from murine melanoma cell lines.
J. Dou (2007)
10.1091/MBC.7.3.383
CD44/chondroitin sulfate proteoglycan and alpha 2 beta 1 integrin mediate human melanoma cell migration on type IV collagen and invasion of basement membranes.
J. R. Knutson (1996)
10.3109/10611869609046255
Evaluation of antitumor activities of hyaluronate binding antitumor drugs: synthesis, characterization and antitumor activity.
K. Akima (1996)
10.1021/BM025651X
On the characterization of pH-sensitive liposome/polymer complexes.
Emmanuelle Roux (2003)
Differences in hyaluronic acid-mediated functions and signaling in arterial, microvessel, Journal of Drug Delivery 11 and vein-derived human endothelial cells
V. B. Lokeshwar (2000)
10.1038/380561A0
Doxorubicin in sterically stabilized liposomes
D. Lasic (1996)
10.1021/JA9627656
Self-assembling amphiphiles for construction of protein molecular architecture
Ying-Ching Yu (1996)
10.1007/BF00300234
Determination of subcutaneous tumor size in athymic (nude) mice
M. Tomayko (2004)
10.1021/BI012071W
Modulation of triple-helical stability and subsequent melanoma cellular responses by single-site substitution of fluoroproline derivatives.
N. B. Malkar (2002)
10.1016/S0005-2736(02)00661-2
Rate of biodistribution of STEALTH liposomes to tumor and skin: influence of liposome diameter and implications for toxicity and therapeutic activity.
G. Charrois (2003)
10.1016/j.jconrel.2011.10.008
Hyaluronan-modified and regular multilamellar liposomes provide sub-cellular targeting to macrophages, without eliciting a pro-inflammatory response.
Yifat Glucksam-Galnoy (2012)
10.1158/1078-0432.CCR-08-1034
CD44 is of Functional Importance for Colorectal Cancer Stem Cells
Lei Du (2008)
10.1083/JCB.111.1.261
Characterization of a synthetic peptide from type IV collagen that promotes melanoma cell adhesion, spreading, and motility
M. Chelberg (1990)
10.1074/jbc.273.1.338
Identification of CD44 Residues Important for Hyaluronan Binding and Delineation of the Binding Site*
J. Bajorath (1998)
10.1016/0014-5793(90)81016-H
Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes
A. Klibanov (1990)
10.1002/(SICI)1097-0134(20000501)39:2<103::AID-PROT1>3.0.CO;2-G
Molecular organization, structural features, and ligand binding characteristics of CD44, a highly variable cell surface glycoprotein with multiple functions
J. Bajorath (2000)
10.1016/J.JCONREL.2007.03.020
Enhanced circulation time and antitumor activity of doxorubicin by comblike polymer-incorporated liposomes.
H. Han (2007)
10.1016/S0169-409X(99)00042-3
Possibility of active targeting to tumor tissues with liposomes.
Maruyama (1999)
Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors.
D. Drummond (1999)
10.1016/0003-2697(80)90269-9
Colorimetric determination of phospholipids with ammonium ferrothiocyanate.
J. C. Stewart (1980)
10.1038/nrd1632
Recent advances with liposomes as pharmaceutical carriers
V. Torchilin (2005)
10.1002/ijc.11615
Loading mitomycin C inside long circulating hyaluronan targeted nano‐liposomes increases its antitumor activity in three mice tumor models
D. Peer (2004)
10.1016/0005-2736(91)90246-5
Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo.
T. Allen (1991)
10.1111/j.1747-0285.2007.00610.x
Effects of Drug Hydrophobicity on Liposomal Stability
D. R. Khan (2008)
10.1016/S0169-409X(99)00041-1
The size of liposomes: a factor which affects their targeting efficiency to tumors and therapeutic activity of liposomal antitumor drugs.
Nagayasu (1999)
10.1021/BC0499477
Adapter protein for site-specific conjugation of payloads for targeted drug delivery.
M. Backer (2004)
Hyaluronanmodified and regular multilamellar liposomes provide subcellular targeting to macrophages, without eliciting a proinflammatory response
Y. Glucksam-Galnoy (2012)
Liposome-encapsulated doxorubicin targeted to CD44: a strategy to kill CD44-overexpressing tumor cells.
R. E. Eliaz (2001)
10.1016/0006-291X(87)91310-6
Stimulation of quiescent 3T3 cells by phosphatidic acid-containing liposomes.
D. Siegmann (1987)
10.1146/ANNUREV.MED.58.062105.204854
Cancer stem cells: models and concepts.
P. Dalerba (2007)
10.1074/jbc.M110.200790
Differential Use of Chondroitin Sulfate to Regulate Hyaluronan Binding by Receptor CD44 in Inflammatory and Interleukin 4-activated Macrophages*
B. Ruffell (2011)
10.1096/fj.08-111484
Production of multivalent protein binders using a self‐trimerizing collagen‐like peptide scaffold
Chia-Yu Fan (2008)
10.1021/JA066929M
Targeted drug delivery utilizing protein-like molecular architecture.
E. Rezler (2007)
10.1038/nm.2304
The cancer stem cell: premises, promises and challenges
H. Clevers (2011)
10.1186/1757-2215-1-4
Ovarian cancer: emerging concept on cancer stem cells
M. P. Ponnusamy (2008)
Doxorubicin in sterically stabilized
D. Lasic (1996)
10.1081/CNV-100103136
Pegylated Liposomal Doxorubicin: Metamorphosis of an Old Drug into a New Form of Chemotherapy
A. Gabizon (2001)
10.1074/JBC.M401584200
Spacrcan Binding to Hyaluronan and Other Glycosaminoglycans
Q. Chen (2004)
Nuclear delivery of doxorubicin via folate-targeted liposomes with bypass of multidrug-resistance efflux pump.
D. Goren (2000)
Cell surface CD44-related chondroitin sulfate proteoglycan is required for transforming growth factor-beta-stimulated mouse melanoma cell motility and invasive behavior on type I collagen.
A. Faassen (1993)
10.1083/JCB.116.2.521
A cell surface chondroitin sulfate proteoglycan, immunologically related to CD44, is involved in type I collagen-mediated melanoma cell motility and invasion
A. Faassen (1992)
10.1081/LPR-100108459
POLY(HPMA)-COATED LIPOSOMES DEMONSTRATE PROLONGED CIRCULATION IN MICE
K. Whiteman (2001)
10.1074/jbc.M800109200
Hyaluronan-CD44 Interaction Activates Stem Cell Marker Nanog, Stat-3-mediated MDR1 Gene Expression, and Ankyrin-regulated Multidrug Efflux in Breast and Ovarian Tumor Cells*
L. Bourguignon (2008)
Complex display of putative tumor stem cell markers in the NCI 60 tumor cell line panel The cancer stem cell : premises , promises and challenges
K. Rilla (2011)
10.1016/0040-4039(96)01685-1
Synthesis and liposome-formation of a thermostable lipid bearing cell adhesion peptide sequence
H. Hojo (1996)
10.1248/CPB.39.1620
Effect of molecular weight in amphipathic polyethyleneglycol on prolonging the circulation time of large unilamellar liposomes.
K. Maruyama (1991)
10.1074/jbc.M109.027466
Hyaluronan-CD44 Interaction with Protein Kinase Cϵ Promotes Oncogenic Signaling by the Stem Cell Marker Nanog and the Production of MicroRNA-21, Leading to Down-regulation of the Tumor Suppressor Protein PDCD4, Anti-apoptosis, and Chemotherapy Resistance in Breast Tumor Cells*
L. Bourguignon (2009)
10.1016/J.BBRC.2005.06.108
Chondroitin sulfate addition to CD44H negatively regulates hyaluronan binding.
B. Ruffell (2005)
10.1074/JBC.M103481200
Hyaluronan Enters Keratinocytes by a Novel Endocytic Route for Catabolism*
R. Tammi (2001)
10.1021/BI982315L
Structure and dynamics of peptide-amphiphiles incorporating triple-helical proteinlike molecular architecture.
Y. C. Yu (1999)
10.1073/pnas.0610298104
Biomimetic amplification of nanoparticle homing to tumors
D. Simberg (2007)
10.1002/stem.324
Complex Display of Putative Tumor Stem Cell Markers in the NCI60 Tumor Cell Line Panel
C. Stuelten (2010)
10.1002/(SICI)1097-0282(1998)47:2<143::AID-BIP3>3.0.CO;2-U
Proteinlike molecular architecture: Biomaterial applications for inducing cellular receptor binding and signal transduction
G. Fields (1998)
10.1016/0005-2760(92)90255-T
Prolonged circulation time in vivo of large unilamellar liposomes composed of distearoyl phosphatidylcholine and cholesterol containing amphipathic poly(ethylene glycol).
K. Maruyama (1992)
10.1111/j.1365-2613.2010.00747.x
Expression of CD176 (Thomsen‐Friedenreich antigen) on lung, breast and liver cancer‐initiating cells
Wei-Ming Lin (2011)
10.1038/sj.bjc.6604242
CD44+CD24− prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis
E. Hurt (2008)
10.1158/0008-5472.CAN-03-0654
Determination and Modeling of Kinetics of Cancer Cell Killing by Doxorubicin and Doxorubicin Encapsulated in Targeted Liposomes
R. E. Eliaz (2004)
10.1074/JBC.M500737200
Regulation of MDR1 Expression and Drug Resistance by a Positive Feedback Loop Involving Hyaluronan, Phosphoinositide 3-Kinase, and ErbB2*♦
S. Misra (2005)
Liposomes: the next generation
J. Jamil (2004)
10.1182/BLOOD-2006-09-048686
Granulocyte colony-stimulating factor enhances bone tumor growth in mice in an osteoclast-dependent manner.
A. Hirbe (2007)
10.1093/GLYCOB/11.7.587
Cell surface-expressed Thomsen-Friedenreich antigen in colon cancer is predominantly carried on high molecular weight splice variants of CD44.
R. Singh (2001)
10.1111/1523-1747.EP12462776
Migration of human melanoma cells on hyaluronate is related to CD44 expression.
L. Thomas (1993)
Liposomes : a practical approach
R. New (1990)



This paper is referenced by
10.1016/j.addr.2015.11.013
Collagen interactions: Drug design and delivery.
Bo An (2016)
10.3389/fimmu.2019.01278
Mechanisms of Action of Novel Drugs Targeting Angiogenesis-Promoting Matrix Metalloproteinases
G. Fields (2019)
10.3390/cells8090984
The Rebirth of Matrix Metalloproteinase Inhibitors: Moving Beyond the Dogma
G. Fields (2019)
10.1016/j.biotechadv.2016.01.004
Nanotechnology-based strategies for combating toxicity and resistance in melanoma therapy.
Adam K. Brys (2016)
Characteristics and side effects of common nanoparticles used in the study of melanoma treatment Nanoparticle
J. Chen (2013)
10.3109/1061186X.2015.1052072
Hyaluronic acid targeting of CD44 for cancer therapy: from receptor biology to nanomedicine*
George Mattheolabakis (2015)
10.1155/2014/895986
Drug Delivery Nanoparticles in Skin Cancers
C. Dianzani (2014)
10.1016/j.ijpharm.2020.120117
Liposomal doxorubicin as targeted delivery platform: Current trends in surface functionalization.
V. Makwana (2020)
10.1038/s41428-019-0234-z
Complex formation of a triple-helical peptide with sodium heparin
Saki Ishida (2019)
10.1021/acs.jmedchem.7b00018
Second Generation Triple-Helical Peptide Inhibitors of Matrix Metalloproteinases.
Manishabrata Bhowmick (2017)
10.2147/IJN.S45429
Applications of nanotechnology for melanoma treatment, diagnosis, and theranostics
J. Chen (2013)
10.1016/B978-0-12-802926-8.00015-X
Nanodelivery of Anticancer Agents in Melanoma
J. Chen (2016)
10.1002/9783527683451.CH7
Bioorthogonal Labeling of Cellular Proteins by Enzymatic and Related Mechanisms
Scott A. Walper (2017)
10.1074/jbc.RA118.003266
Dissecting MMP P10′ and P11′ subsite sequence preferences, utilizing a positional scanning, combinatorial triple-helical peptide library
Michal Tokmina-Roszyk (2018)
10.3389/fbioe.2020.00069
Targeted Drug Delivery via the Use of ECM-Mimetic Materials
Jeongmin Hwang (2020)
10.1080/1061186X.2016.1274996
Biocompatible complex coated with glycosaminoglycan for gene delivery
Marie Iwanaga (2017)
10.1016/j.matbio.2015.01.002
New strategies for targeting matrix metalloproteinases
G. Fields (2015)
10.1186/s12885-015-1251-8
The involvement of insulin-like growth factor 2 binding protein 3 (IMP3) in pancreatic cancer cell migration, invasion, and adhesion
Clarissa C Pasiliao (2015)
10.1007/978-1-4939-9095-5_17
Methods for the Construction of Collagen-Based Triple-Helical Peptides Designed as Matrix Metalloproteinase Inhibitors.
G. Fields (2019)
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