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Lamellar Mitogen-Activated Protein Kinase and Hypoxia Signaling in a Sepsis-Related Laminitis Model and a Novel Supporting Limb Laminitis Model

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Lamellar Mitogen-Activated Protein Kinase and Hypoxia Signaling in a Sepsis-Related Laminitis Model and a Novel Supporting Limb Laminitis Model Lamellar Mitogen-Activated Protein Kinase and Hypoxia Signaling in a Sepsis-Related Laminitis Model and a Novel Supporting Limb Laminitis Model THESIS Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University Alison K Gardner DVM, BS, MS Graduate Program in Comparative and Veterinary Medicine The Ohio State University 2015 Thesis Committee Members James Belknap DVM PhD, Advisor Prosper Boyaka PhD Teresa Burns DVM PhD Ramiro Toribio DVM PhD Copyright by Alison K Gardner 2015 Abstract The term laminitis refers to dysadhesion of the lamellar basilar epithelial cell (LBEC) from the basement membrane, resulting in distal displacement of the third phalanx. Multiple etiologies of laminitis exist, which can be grouped into three broad categories: equine metabolic syndrome-associated laminitis, sepsis- related laminitis (SRL) and supporting limb laminitis (SLL). This thesis centers on two different laminitis models, the first being based on sepsis-related laminitis and the second being a novel model for supporting limb laminitis. Sepsis-related laminitis, an often fatal sequela in critical equine patients secondary to endotoxemia and sepsis-potentiating diseases, appears to be due to aberrant laminar cell signaling reportedly involving inflammatory and possibly other signaling pathways. The only documented effective treatment for sepsis- related laminitis is regional deep hypothermia (RDH, foot submerged in ice water). Mitogen-activated protein kinases (MAPKs), activated in inflammation or downstream of growth factor signaling, are potential therapeutic targets for many disease processes. Our objectives were to assess MAPK signaling in laminar tissue in a model of sepsis-related laminitis and to determine the effect of RDH on MAPK signaling. Lamellar concentrations of MAPKs were assessed from two ii groups of horses receiving a carbohydrate-overload with samples collected at different time points versus a control. Another set was taken from a carbohydrate-overload model where one front limb was treated with RDH while the other remained at ambient temperature. Lamellar concentrations and cellular localization of the MAPKs and the signaling proteins of the interconnected protein kinase B (Akt)/Phosphoinositide 3 kinase (PI3k)/mammalian target of rapamycin (mTOR) pathway were assessed. Whereas no change in lamellar p38 MAPK was found in the CHO models, lamellar concentrations of growth factor-related signaling molecules including the phosphorylated/activated MAPK, extracellular signal-regulated kinase (ERK) 1/2 and its downstream effector ribosomal protein S6 (RPS6) were increased (p<0.05) at the onset of laminitis, as was the MAPK stress-activated protein kinase/c-jun N terminal (SAPK/JNK) 1/2, the cellular negative-energy balance signaling protein AMP-activated protein kinase α (AMPKα), and Akt. Hypothermia did not inhibit ERK 1/2, but did cause a decrease in RPS6 phosphorylation/activation but an increase in SAPK/JNK 1/2 phosphorylation/activation. Signaling related to growth factor-related pathways should be further investigated in SRL, especially since it has been implicated in cell-cell dysadhesion and upregulation of the ERK 1/2 pathway. The pathophysiology of equine supporting limb laminitis (SLL), a common and often fatal complication of equine orthopedic disease, is poorly understood. Often horses survive the initial catastrophic trauma, e.g. fracture, only to succumb to fulminant failure of the contralateral limb. Suggested causes of iii lamellar failure include inflammatory injury, hypoxia and mechanical strain. We hypothesized that lamellar hypoxia occurs in the supporting limb (SL) resulting in increase in lamellar hypoxia-inducible factor-1α (HIF-1α). A novel model of SLL was used in this study in which a custom shoe insert causing instability to the sole surface upon weight bearing was placed on one forelimb of horses resulting in excessive weighting of the contralateral forelimb (SL). Lamellae were harvested and immediately snap-frozen from all four limbs 48 h post-application of the shoe. Western immunoblotting and real time-quantitative PCR (qPCR) were used to assess markers of hypoxia (HIF-1α) inflammation and stretch. The only change noted was an increase (P<0.05) in lamellar HIF-1α protein concentrations in the SL compared to one hindlimb and a trending increase in the other. Genes including those indicated in stretch, metabolism and inflammation were not upregulated, nor was HIF-1α mRNA. These results indicate that lamellar hypoxia and HIF-1α may play a central role in SLL and future research should focus on therapeutic options, including novel shoeing options on the SL which may allow increased vascular oxygen delivery to the distal limb. HIF-1α may have value as a biomarker of lamellar hypoxia and be used to assess the efficacy of SLL treatments. The two models (CHO and SLL) exhibit differences between the arms of sepsis-related and supporting limb laminitis. However, further work must be done on cellular growth factor signaling and metabolic pathways, as recent evidence shows that while SRL and SLL have differing properties in MAPK, iv Akt/PI3k/mTOR, and HIF-1α activation as well as pro-inflammatory cyotokine gene expression, RPS6 may play a role in dysadhesion of the epidermal lamellae. v Dedication To my family, who have sacrificed so much. To my mother, who reminds me daily what strength and grace can overcome. vi Acknowledgements First and foremost, I have to thank Dr. Jim Belknap, my advisor, for his guidance both through the research process and through my residency. I have always felt I have had his support, even on the thirtieth time he had to explain calculating fold change. It is difficult training a nascent pony doctor to be well- versed in cellular-signaling, but he certainly is willing to try, always with a sense of humor. Thank you to my committee members, Drs. Prosper Boyaka, Teresa Burns and Ramiro Toribio for being on my committee. I am equally indebted to Mauria Watts. She has been my tutor in bench top protocols, my editor and a guide both in the lab and out. Mauria is a good friend and amazing asset, and any student who works under her is lucky to do so. I would also like to thank Dr. Teresa Burns for her guidance and help with nearly every step in the process. Dr. Burns is always available and so very kind, whether I am asking a stupid internal medicine question or equally ignorant statistical evaluation one. Thanks also to Heather Lane and Dr. Cassie Quinlan for sample collection, and to Dr. Carlin Kelly for the research she had started on p38 MAPK. Thanks also to Dr. Andrew Van Eps and Dr. Britta Leise for vii lamellar tissue used in the CHO and RDH models. Thank you to Tim Vojt for his work on the HIF-1α figures. Thank you also to my family and my partner, Mark, for all their patience and fortitude. Thank you to my other clinicians, my resident mates and the wonderful technicians for their patience with me during this residency. viii Vita Ohio State University, graduate research associate…June 2012-present Colorado State University, DVM…………................….………...May 2011 Colorado State University, MS……………………..………….August 2007 Colorado State University, BS…………………………………….May 2006 Publications A.K. Gardner, M.R. Watts, T. A. Burns, J. K. Belknap. Abstract: Examining laminar signaling in a model of supporting limb laminitis. Journal of Equine Veterinary Science, 2013 v33 n10: 862-863 presented at the 2013 ACVS Symposium B.S. Leise, R.R. Faleiros, T.A. Burns, A.K. Gardner, M.A. Watts, S.J. Black, R. Geor, L.J. McCutcheon, A. van Eps, C.C. Pollitt, S. Eades, P.J. Johnson, and J.K. Belknap. Inflammation in laminitis: the “itis” in laminitis may not pertain to all.Journal of Equine Veterinary Science, 2013 v33 n10: 860 ix Fields of Study Major Field: Comparative and Veterinary Medicine x Table of Contents Abstract…………………………………………………………………………………...ii Dedication……………………………………………………………………………….vi Acknowledgements…………………………………………………………………….vii Vita……………………………………………………………………………………….ix List of Figures…………………………………………………………………………..xii CHAPTER 1. Introduction………………………………………………………………1 1.1 Structure and Function of the Equine Lamellae………………...………1 1.2 Structural Failure in Laminitis……………………………………………..9 1.3 Equine Metabolic-Syndrome-Associated Laminitis…………………...11 1.4 Sepsis-Related Laminitis………………………………………………...12 1.5 Mitogen-Activated Protein Kinase Signaling (MAPK) and the Akt/PI3/mTOR Signaling Pathways…………………………………….16 1.6 Supporting Limb Laminitis……………………………………………….25 CHAPTER 2. MAPK and the Akt/PI3/mTOR Signaling Pathways in a Carbohydrate-Overload (CHO) Model and in Response to Regional Deep Hypothermia (RDH)……………………………………………………………………30 2.1 Materials and Methods: CHO and RDH Models……………………….30 2.2 Results: CHO and RDH Models…………………………………………34 2.3 Discussion: CHO and RDH Models……………………………………..53 CHAPTER 3.Hypoxia Signaling in a Novel Supporting Limb Laminitis (SLL) Model……………………………………………………………………………………59 3.1 Materials and Methods: SLL Model……………………………………..59 3.2 Results: SLL Model……………………………………………………….66 3.3 Discussion: SLL Model…………………………………………………...71 CHAPTER 4: Discussion and Conclusions…………………………………………75 4.1 Overview of Results from Two Laminitis Models……………………...75 4.2 MAPK Data………………………………………………………………..77 4.3 Moving Away from Pro-Inflammatory Gene Expression as Sole Causation in Sepsis-Related Laminitis……………………………………………..80 xi 4.4 A Potential Role of the Ras/ERK 1/2 PI3/Akt/mTOR Pathway and RPS6……………………………………………………………………………………81
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