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Phytochemical Antioxidants Induce Membrane Lipid Signaling in Vascular

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Phytochemical Antioxidants Induce Membrane Lipid Signaling in Vascular Phytochemical Antioxidants Induce Membrane Lipid Signaling in Vascular Endothelial Cells THESIS Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Jordan Douglas Secor Graduate Program in Pathology The Ohio State University 2012 Master's Examination Committee: Dr. Narasimham Parinandi, Co-advisor Dr. W. James Waldman, Co-advisor Copyright by Jordan Douglas Secor 2012 Abstract Isolated phytochemicals have recently been increasingly consumed worldwide for prevention of cancer, cardiovascular and cerebrovascular diseases, and other ailments. Hence, the phytochemical nutraceuticals have been thoroughly investigated as anticancer chemotherapeutics and use as dietary antioxidant continues to grow. Phytochemical polyphenols including baicalein, myricetin, rutin, and resveratrol are among a number of plant extracts believed to possess potential therapeutic efficacies. The putative anticancer effects of these natural compounds are believed to result, in part, from prevention of eicosanoid production through inhibition of 12-lipoxygenase (12-LOX). However, the mechanisms underlying these observations are not entirely clear and the effects of these compounds on noncancerous cells such as the vascular endothelial cells (ECs) are largely yet to be investigated. Few preliminary studies have reported that some isolated phytochemical antioxidants may actually act through a prooxidant mechanism. Earlier we have reported that prooxidants activate phospholipase D (PLD) signaling in ECs through depletion of intracellular thiols, generation of reactive oxygen species (ROS), and lipid peroxidation. We have also shown that oxidant-induced activation of PLD, which generates the potent bioactive lipid signaling molecule phosphatidic acid (PA), results in mitogenesis, cellular trafficking, cytoskeletal rearrangements and, ultimately, cytotoxicity. Consequently, here we used our established, bovine pulmonary artery EC ii (BPAEC) model to examine whether the phytochemical polyphenol treatment would modulate lipid signaling in the vascular ECs. We hypothesized that baicalein, a polyphenolic phytochemical derived from Scutellaria baicalensis, would induce activation of PLD through the loss of intracellular thiols, generation of ROS, induction of peroxidation of membrane phospholipids in a prooxidant mechanism in the vascular endothelial cells in culture, ultimately leading to cytotoxicity regulated by the PLD- derived PA. Hence, in this study, we investigated this potential mechanism through (i) indexing PLD activity by measuring PA formation and PLD1 and PLD2 in situ translocation and phosphorylation (ii) measuring formation of intracellular ROS (iii) analyzing global and PLD2-specific tyrosine phosphorylation (iv) measuring loss of intracellular thiols (both GSH and total thiols) (v) quantifying 8-isoprostane release as a measure of lipid peroxidation and (vi) measuring LDH release as an index of cytotoxicity. With the use of different specific pharmacological inhibitors, we investigated the mechanism of PLD activation in BPAECs as quantified by the formation of PA. Furthermore, we observed this mechanism to be dependent on and attenuable through inhibition of the following: (i) PLD activation with the PLD-specific inhibitor FIPI (ii) loss of thiols through the thiol-protectants DTT and NAC (iii) free radical formation through propyl gallate, MnTBAP, and MnTMPyP (iv) labile iron through the iron chelator desferal (v) calcium loss through BAPTA and (vi) protein tyrosine kinase (PTyK) signaling by the PTyK-specific inhibitors erbstatin, damnacanthal, tyrophostin AG34, and genistein. Cumulatively, this study revealed for the first time that the phytochemical polyphenolic 12-LOX inhibitor, baicalein induced activation of PLD in iii the vascular ECs through thiol-redox-dependent oxidant signaling and protein tyrosine kinase leading to the bioactive lipid (PA)-mediated cytotoxicity. Consequently, the cancer-specific chemotherapeutic efficacy, anti-angiogenic action, and antioxidant potential of baicalein and other polyphenolic phytochemicals must be reconsidered. iv Acknowledgments I would like to thank Dr. Narasimham Parinandi for his guidance and support as a mentor in my continuing development as a research scientist. My success is a result of his efforts. Also, I would like to thank Dr. Jim Waldman for affording me the opportunity to pursue a Master of Science degree. I am forever grateful. Finally, I would like to thank Dr. Sainath Kotha for training me by example to be an independent and innovative scientist. Attaining Dr. Kotha’s clinical acumen and research excellence are lifetime goals. v Vita May 2006 .......................................................Ada High School 2010................................................................B.S. Biology, The Ohio State University Publications Secor, J., Kotha, S., Gurney, T., Patel, R., Kefauver, N., Gupta, N., Morris, A., Haley, B., and Parinandi, N. 2011. Novel lipid-soluble thiol-redox antioxidant and heavy metal chelator, N,N'-bis(2-mercaptoethyl)isophthalamide (NBMI) and phospholipase D- specific inhibitor, 5-fluoro-2-indolyl des-chlorohalopemide (FIPI) attenuate mercury- induced lipid signaling leading to protection against cytotoxicity in aortic endothelial cells. International Journal of Toxicology 30, 619-638. Kotha, S., Secor, J., Abbott, J., Gurney, T., Patel, R., Morris, A., Elton, T., Natarajan, V., and Parinandi, N. 2012. Angiotensin II-Induced Vascular Smooth Muscle Cell Proliferation is Mediated by Phosphatidic Acid: Role of ERK-regulated Phospholipase D Signaling. Submitted for publication in the J. Biological Chemistry. Reviews: vi Malireddy, S., Kotha, S., Secor, J., Gurney, T., Abbott, J., Maulik, G., Maddipati, K., Parinandi, and N. 2012. Phytochemical Antioxidants Modulate Mammalian Cellular Epigenome: Implications in Health and Disease. Antioxidants and Redox Signaling [epub ahead of print]. Book Chapters: Kotha, S., Secor, J., Malireddy, S., and Parinandi, N. 2012. Bioactive Phospholipid Mediators of Inflammation. Chronic Inflammation: Molecular Pathophysiology, Nutritional and Therapeutic Interventions. Cenveo Publishers. Fields of Study Major Field: Pathology vii Table of Contents Abstract ........................................................................................................................... ii-iv Acknowledgments............................................................................................................... v Vita .............................................................................................................................. vvi-vii List of Figures ............................................................................................................... ixx-x Chapter 1: Introduction .............................................................................................. pp. 1-5 Chapter 2: Materials and Methods ........................................................................... pp. 6-13 Chapter 3: Results .................................................................................................. pp. 14-23 Chapter 4: Figures .................................................................................................. pp. 24-51 Chapter 5: Discussion ............................................................................................ pp. 55-62 Chapter 7: References ............................................................................................ pp. 63-65 viii List of Figures 1. Baicalein Structure 2. Baicalein Induces PLD Activation in Endothelial Cells A. Time Course and Dose Response in BLMVECs B. Time Course and Dose Response in BPAECs C. Kaempferol Does Not Activate PLD in BPAECs D. FIPI Inhibits Baicalein-Induced PLD Activation 3. Thiol-Protectants Inhibit Baicalein-Induced PLD Activation in Endothelial Cells A. DTT Inhibits Baicalein-Induced PLD Activation B. NAC Inhibits Baicalein-Induced PLD Activation 4. Free Radical Quenchers and Antioxidants Inhibit Baicalein-Induced PLD Activation in Endothelial Cells A. Propyl Gallate Inhibits Baicalein-Induced PLD Activation B. MnTBAP Inhibits Baicalein-Induced PLD Activation C. MnTMPyp Inhibits Baicalein-Induced PLD Activation 5. The Iron Chelator Desferal, but Not DTPA or EDTA, Attenuates Baicalein- Induced PLD Activation in Endothelial Cells A. DTPA Fails to Attenuate Baicalein-Induced PLD Activation B. EDTA Fails to Attenuate Baicalein-Induced PLD Activation C. Desferal Inhibits Baicalein-Induced PLD Activation 6. Intracellular Calcium Chelators Inhibit Baicalein-Induced PLD Activation in Endothelial Cells A. BAPTA Inhibits Baicalein-Induced PLD Activation 7. Protein Tyrosine Kinase Inhibitors Attenuate Baicalein-Induced PLD Activation in Endothelial Cells A. Erbstatin and Damnacanthal Inhibit Baicalein-Induced PLD Activation B. Tyrophostin AG34 Inhibits Baicalein-Induced PLD Activation 8. Baicalein Induces Translocation of PLD in Endothelial Cells A. Baicalein Induces Transolcation of PLD1 (confocal) B. Baicalein Induces Transolcation of PLD2 (confocal) 9. Baicalein Induces Tyrosine Phosphorylation in Endothelial Cells A. Baicalein Induces Global Tyrosine Phosphorylation (western) B. Baicalein Induces PLD1 Tyrosine Phosphorylation (confocal) C. Baicalein Induces PLD2 Tyrosine Phosphorylation (confocal) 10. Baicalein Causes Generation of ROS in Endothelial Cells ix A. Baicalein Causes Generation of DHE (confocal) 11. NAC Protects Against
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