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A2ff58402e845f07ce08114af6bd International Journal of Molecular Sciences Article Characterizing Sphingosine Kinases and Sphingosine 1-Phosphate Receptors in the Mammalian Eye and Retina Hunter Porter 1,†, Hui Qi 1,†, Nicole Prabhu 1,†, Richard Grambergs 2, Joel McRae 1, Blake Hopiavuori 1 and Nawajes Mandal 1,2,* 1 Department of Ophthalmology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA; [email protected] (H.P.); [email protected] (H.Q.); [email protected] (N.P.); [email protected] (J.M.); [email protected] (B.H.) 2 Departments of Ophthalmology, Anatomy and Neurobiology, University of Tennessee Health Sciences Center, Memphis, TN 38163, USA; [email protected] * Correspondence: [email protected]; +1-901-448-7740 † Equally contributing author. Received: 19 November 2018; Accepted: 27 November 2018; Published: 5 December 2018 Abstract: Sphingosine 1-phosphate (S1P) signaling regulates numerous biological processes including neurogenesis, inflammation and neovascularization. However, little is known about the role of S1P signaling in the eye. In this study, we characterize two sphingosine kinases (SPHK1 and SPHK2), which phosphorylate sphingosine to S1P, and three S1P receptors (S1PR1, S1PR2 and S1PR3) in mouse and rat eyes. We evaluated sphingosine kinase and S1P receptor gene expression at the mRNA level in various rat tissues and rat retinas exposed to light-damage, whole mouse eyes, specific eye structures, and in developing retinas. Furthermore, we determined the localization of sphingosine kinases and S1P receptors in whole rat eyes by immunohistochemistry. Our results unveiled unique expression profiles for both sphingosine kinases and each receptor in ocular tissues. Furthermore, these kinases and S1P receptors are expressed in mammalian retinal cells and the expression of SPHK1, S1PR2 and S1PR3 increased immediately after light damage, which suggests a function in apoptosis and/or light stress responses in the eye. These findings have numerous implications for understanding the role of S1P signaling in the mechanisms of ocular diseases such as retinal inflammatory and degenerative diseases, neovascular eye diseases, glaucoma and corneal diseases. Keywords: S1P; sphingosine 1-phosphate; S1PR1; sphingosine 1-phosphate receptor 1; S1PR2; S1PR3; sphingosine kinase 1; SPHK2; retina; eye 1. Introduction Sphingolipids play diverse roles in the biology of cells and tissues [1]. As structural lipids, they are essential to maintaining membrane fluidity and organizing lipid rafts [2,3]. However, their role is far from limited to membrane dynamics. The various species of sphingolipids are found throughout the cell including in the nucleus, cytoplasm, and in the extracellular space as signaling molecules [3–6]. Bioactive sphingolipids such as sphingosine 1-phosphate (S1P) and ceramide (Cer) are now recognized as important mediators of many basic cellular processes including cell migration, survival, contraction, proliferation, gene expression and various cell-cell interactions [1,5,7–15]. The scope of the sphingolipid system’s impact on mammalian biology has proven to be impressive due to the complexity of the “sphingolipid rheostat” and the many signaling pathways that sphingolipids are involved in. The sphingolipid rheostat is comprised of dozens of enzymes that constantly shift concentrations of sphingolipids such as sphingomyelin (SM), Cer and sphingosine (Sph) by metabolizing them into Int. J. Mol. Sci. 2018, 19, 3885; doi:10.3390/ijms19123885 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2018, 19, 3885 2 of 18 other sphingolipid species. Ceramides and S1P are potent signaling molecules, which the sphingolipid rheostat can generate to respond to a stimulus or use as intermediates toward the degradation pathway. S1P is generated from sphingosine by sphingosine kinases 1 and 2 (SPHK1/SPHK2). Mice deficient in both SPHK1 and SPHK2 have many vascular and neuronal deficits during the development and are not viable past E13.5 [16]. SPHK1 and SPHK2 single knockout animals generally have no phenotype and are thought to compensate with the remaining kinase. However, knocking out SPHK2 is sufficient to reduce resilience to oxygen-induced retinopathy [17]. Meanwhile, the S1P produced by the two kinases has shown myriad roles in retinal development and function. S1P has shown to be essential for photoreceptor development [18] and Muller glia migration [19]. After development, modulating S1P has shown benefits in preventing immune cell migration and neovascularization after insult. The biological effects of S1P are largely attributed to its high-affinity association with receptors present on various cell types. S1P receptors are divided into five subgroups (S1PR1-5), which are G-protein-coupled receptors with unique expression patterns and roles in cell signaling [20–24]. S1PR1 is the most well studied and is present on endothelial cells, B-cells and T-cells. S1PR1 is also an essential receptor for influencing blood vessel development and maturation [21,25,26]. S1PR1 knockout animals are nonviable. S1PR2 and 3 are also ubiquitously expressed [20–24] and important for proper vascular development [27,28]. S1PR2 is important for cell migration [29] and S1PR2 mutations induce hearing loss by disrupting endocochlear potential gradients [30]. S1PR3 has demonstrated an important role in a bacterial infection response [31], nociception and itching sensation [32]. S1PR4 and S1PR5 expression is more restricted and they are mostly found on the cells of the immune and nervous systems, respectively [33,34]. S1PR4 is essential to differentiation of dendritic cells [35] and is important to immune cell chemoattraction [36]. S1PR5 is important in cell migration and, by selectively modulating its activity, can ameliorate demyelination [37] and alter the integrity of the blood brain barrier [38]. In summary, S1P receptors are essential for immune cell response modulation, cell migration, and vascular development and maintenance. These functions are critical to retinal development and survival, but their role in the eye is poorly understood. In the eye, S1P can protect neural cells from apoptosis by inhibiting synthesis of its precursor ceramide, which is a pro-death signaling molecule [5,39–43]. We have previously shown that targeting S1P receptors with FTY-720, which is marketed as a drug for multiple sclerosis, can delay retinal degeneration in light damage and genetic models [44,45]. Ocular tissues outside the retina such as the cornea and retinal pigment epithelium (RPE) have shown S1P receptor expression with functions important to controlling fibrotic responses [46]. Modulating the S1P receptor signaling with FTY-720 has also shown to be beneficial in ocular autoimmune conditions such as uveitis [47]. In the retina proper, S1P is critical to photoreceptor development [18], axonal guidance [48] and survival of retinal ganglion cells in glaucoma [49]. Given the numerous effects of S1P receptors showing translation into ocular development and pathology, we have identified a critical need to understand the distributions of both S1P receptors and sphingosine kinases in the eye. As S1P receptor modulation has shown benefits in counteracting retinal degeneration, we also studied how the expression of S1P-producing sphingosine kinases and S1P receptors changes over time in cases of retinal damage induced by intense light stress. Characterizing S1P signaling in ocular development and stress responses will deepen our understanding of eye health and diseases and potentially identify novel pathways for therapeutic intervention. 2. Results 2.1. Distribution and Expression of Sphingosine Kinase (Sphk) and Sphingosine 1-Phosphate Receptor (S1pr) mRNA in Rat Tissue To understand the roles of S1P signaling in the eye, we first explored the expression of relevant protein coding transcripts throughout the body. Using qRT-PCR, we assayed the expression and distribution of S1P-producing enzymes and the major S1P receptors in various tissues from adult SD rats. SPHK2 is corroborated as a major S1P-producing enzyme with high expression across all Int. J. Mol. Sci. 2018, 19, x FOR PEER REVIEW 3 of 18 Int.distribution J. Mol. Sci. 2018 of S1P-producing, 19, 3885 enzymes and the major S1P receptors in various tissues from adult3 of SD 18 rats. SPHK2 is corroborated as a major S1P-producing enzyme with high expression across all assayed tissues. At the same time, SPHK1 was expressed primarily in ovary and kidney tissue with assayedminimal tissues.expression At thein most same other time, tissues—n SPHK1 wasotably expressed the brain primarily and retina in ovary(Figure and 1A). kidney S1pr1 tissuewas highly with minimalexpressed expression in the hindbrain, in most othermoderately tissues—notably expressed thein the brain forebrain, and retina retina, (Figure heart,1A). lungsS1pr1 andwas spleen, highly expressedand minimally in the hindbrain,expressed moderatelyin the liver, expressed skin and in testes. the forebrain, S1pr3 was retina, moderately heart, lungs expressed and spleen, in andthe minimallyforebrain, retina, expressed liver, in heart, the liver, lungs, skin testes and testes.and kidneyS1pr3 wasand moderatelyin retinal pigment expressed epithelium-choroid in the forebrain, retina,(RPE-choroid) liver, heart, tissue. lungs, S1pr2 testes and and S1pr5 kidney showed and inminimal retinal pigmentexpression epithelium-choroid in the tissues analyzed (RPE-choroid) (Figure tissue.1B). S1pr2 and S1pr5 showed minimal expression in the tissues analyzed (Figure1B).
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