C-Terminal p53 Palindromic Tetrapeptide Restores Full Apoptotic Function to Mutant p53 Cancer Cells In Vitro and In Vivo.

Bax Fas ROS apoptosis breast cancer p53 p53 peptide

Journal

Biomedicines
ISSN: 2227-9059
Titre abrégé: Biomedicines
Pays: Switzerland
ID NLM: 101691304

Informations de publication

Date de publication:
05 Jan 2023
Historique:
received: 08 05 2022
revised: 25 07 2022
accepted: 15 08 2022
entrez: 21 1 2023
pubmed: 22 1 2023
medline: 22 1 2023
Statut: epublish

Résumé

We previously demonstrated that a synthetic monomer peptide derived from the C-terminus of p53 (aa 361−382) induced preferential apoptosis in mutant p53 malignant cells, but not normal cells. The major problem with the peptide was its short half-life (half-life < 10 min.) due to a random coil topology found in 3D proton NMR spectroscopy studies. To induce secondary/tertiary structures to produce more stability, we developed a peptide modelled after the tetrameric structure of p53 essential for activation of target genes. Starting with the above monomer peptide (aa 361−382), we added the nuclear localization sequence of p53 (aa 353−360) and the end of the C-terminal sequence (aa 383−393), resulting in a monomer spanning aa 353−393. Four monomers were linked by glycine to maximize flexibility and in a palindromic order that mimics p53 tetramer formation with four orthogonal alpha helices, which is required for p53 transactivation of target genes. This is now known as the 4 repeat-palindromic-p53 peptide or (4R-Pal-p53p). We explored two methods for testing the activity of the palindromic tetrapeptide: (1) exogenous peptide with a truncated antennapedia carrier (Ant) and (2) a doxycycline (Dox) inducer for endogenous expression. The exogenous peptide, 4R-Pal-p53p-Ant, contained a His tag at the N-terminal and a truncated 17aa Ant at the C-terminal. Exposure of human breast cancer MB-468 cells and human skin squamous cell cancer cells (both with mutant p53, 273 Arg->His) with purified peptide at 7 µM and 15 µM produced 52% and 75%, cell death, respectively. Comparatively, the monomeric p53 C-terminal peptide-Ant (aa 361−382, termed p53p-Ant), at 15 µM and 30 µM induced 15% and 24% cell death, respectively. Compared to the p53p-Ant, the exogenous 4R-pal-p53p-Ant was over five-fold more potent for inducing apoptosis at an equimolar concentration (15 µM). Endogenous 4R-Pal-p53p expression (without Ant), induced by Dox, resulted in 43% cell death in an engineered MB468 breast cancer stable cell line, while endogenous p53 C-terminal monomeric peptide expression produced no cell death due to rapid peptide degradation. The mechanism of apoptosis from 4R-Pal-p53p involved the extrinsic and intrinsic pathways (FAS, caspase-8, Bax, PUMA) for apoptosis, as well as increasing reactive oxygen species (ROS). All three death pathways were induced from transcriptional/translational activation of pro-apoptotic genes. Additionally, mRNA of p53 target genes (Bax and Fas) increased 14-fold and 18-fold, respectively, implying that the 4R-Pal-p53p restored full apoptotic potential to mutant p53. Monomeric p53p only increased Fas expression without a transcriptional or translational increase in Fas, and other genes and human marrow stem cell studies revealed no toxicity to normal stem cells for granulocytes, erythrocytes, monocytes, and macrophages (CFU-GEMM). Additionally, the peptide specifically targeted pre-malignant and malignant cells with mutant p53 and was not toxic to normal cells with basal levels of WT p53.

Identifiants

pubmed: 36672645
pii: biomedicines11010137
doi: 10.3390/biomedicines11010137
pmc: PMC9855826
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : Manelski Family Foundation, Chemotherapy Foundation Award, Susan Grant Kaplansky Memorial Fund, Herbert Pardes Scholar Award, Herbert Irving Scholar Award,Columbia University WAR grants to RLF and NIH R01OH07590 grant to PWBR
ID : NIH R01 CA 82528

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Auteurs

Robert L Fine (RL)

Experimental Therapeutics Program, Division of Medical Oncology, College of Physicians and Surgeons of Columbia University, New York, NY 10314, USA.

Yuehua Mao (Y)

Experimental Therapeutics Program, Division of Medical Oncology, College of Physicians and Surgeons of Columbia University, New York, NY 10314, USA.

Richard Dinnen (R)

Experimental Therapeutics Program, Division of Medical Oncology, College of Physicians and Surgeons of Columbia University, New York, NY 10314, USA.

Ramon V Rosal (RV)

Department of Environmental Health Sciences, Mailman School of Public Health of Columbia University, New York, NY 10314, USA.

Anthony Raffo (A)

Experimental Therapeutics Program, Division of Medical Oncology, College of Physicians and Surgeons of Columbia University, New York, NY 10314, USA.

Uri Hochfeld (U)

Experimental Therapeutics Program, Division of Medical Oncology, College of Physicians and Surgeons of Columbia University, New York, NY 10314, USA.

Patrick Senatus (P)

Department of Neurosurgery, Neurologic Institute of New York, Columbia University Medical Center, New York, NY 10032, USA.

Jeffrey N Bruce (JN)

Department of Neurosurgery, Neurologic Institute of New York, Columbia University Medical Center, New York, NY 10032, USA.

Gwen Nichols (G)

Experimental Therapeutics Program, Division of Medical Oncology, College of Physicians and Surgeons of Columbia University, New York, NY 10314, USA.

Hsin Wang (H)

Department of Chemistry, College of Staten Island, 2800 Victory Boulevard, New York, NY 10314, USA.

Yongliang Li (Y)

Department of Environmental Health Sciences, Mailman School of Public Health of Columbia University, New York, NY 10314, USA.

Paul W Brandt-Rauf (PW)

Department of Environmental Health Sciences, Mailman School of Public Health of Columbia University, New York, NY 10314, USA.
School of Biomedical Engineering, Science and Health Systems, Drexel University, Philadelphia, PA 19104, USA.

Classifications MeSH