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Role of Mitochondrial Uncoupling Protein 4 in Rat Inner Ear

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Role of Mitochondrial Uncoupling Protein 4 in Rat Inner Ear Molecular and Cellular Neuroscience 47 (2011) 244–253 Contents lists available at ScienceDirect Molecular and Cellular Neuroscience journal homepage: www.elsevier.com/locate/ymcne Role of mitochondrial uncoupling protein 4 in rat inner ear Alina Smorodchenko a,c, Anne Rupprecht a,c, Julia Fuchs b, Johann Gross b, Elena E. Pohl a,c,⁎ a Department of Physiology and Biophysics, University of Veterinary Medicine, Vienna, Austria b Department of Othorhinolaryngology, Charité—Universitaetsmedizin Berlin, Germany c Institute of Cell Biology and Neurobiology, Charité—Universitaetsmedizin Berlin, Germany article info abstract Article history: The uncoupling protein 4 (UCP4) belongs to the mitochondrial anion transporter family. Protein tissue Received 3 September 2010 distribution and functions are still a matter of debate. Using an antibody we have previously shown that UCP4 Revised 3 March 2011 appears in neurons and to a lesser extent in astrocytes of murine neuronal tissue as early as days 12–14 of Accepted 3 March 2011 embryonic development (Smorodchenko et al., 2009). Here we demonstrated for the first time that Available online 11 March 2011 neurosensory cells such as hair cells of the inner ear and mechanosensitive Merkel cells in skin also express a significant amount of UCP4. We tested the hypothesis about whether UCP4 contributes to the regulation of Keywords: Mitochondrial membrane protein oxidative stress using the model of oxygen deprivation. For this we compared the protein expression level in Voltage dependent anion channel freshly isolated explants of organ of Corti, modiolus and stria vascularis from neonatal rats with explants Spiral ganglion neurons cultured under hypoxia. Western blot analysis revealed that the UCP4 level was not increased under hypoxic Cochlea development conditions, when compared to the mitochondrial outer membrane protein VDAC or to the anti-oxidative Hypoxia enzyme SOD2. We moreover demonstrated that UCP4 expression is differently regulated during postnatal Oxidative stress stages and is region-specific. We hypothesized that UCP4 may play an important role in functional maturation Reactive oxygen species of the rat inner ear. Hair cells © 2011 Published by Elsevier Inc. Merkel cell Sensory cell Introduction of fetal and adult animals with the maximal content in the cortex. Based on the finding that UCP4 expression coincided with the UCP4 is a mitochondrial inner membrane protein, which belongs beginning of neurogenesis, we recently hypothesized that the to the anion carrier family. The physiological role of UCP4 is still not protein may be involved in neuronal cell differentiation and/or clear, but several putative functions such as a regulation of free apoptosis (Smorodchenko et al., 2009). Zhang et al. (2006) earlier radicals production and calcium homeostasis (Chan et al., 2006; Wu reported that the overexpression of UCP4 in preadipocyte inhibits et al., 2009), involvement in apoptosis in the mammalian brain (Mao their differentiation into adipocytes, but stimulates preadipocyte et al., 1999; Hanak and Jezek, 2001), modulation of neuronal activity proliferation and protects preadipocytes from apoptosis induced by (Mattson and Liu, 2003) and participation in thermogenesis (Liu et al., serum deprivation. 2006) are in discussion. UCP4 mRNA in the rat inner ear was first described by Recently, we designed a pure affinity anti-UCP4 antibody and Kitahara et al. (Kitahara et al., 2004). In subsequent reports showed that the protein is mainly expressed in neuronal mito- Kitahara et al. (Kitahara et al., 2005, 2007) claimed that different chondria and to a lesser extent in astrocytes (Smorodchenko et al., UCP subfamily members including UCP4 contribute to the 2009). The protein expression level varied in different brain regions neuroprotection against the pharmacologically (kanamycin intox- ication) and mechanically (labyrinthectomy) induced oxidative damage and have a signaling role for the neuromodulation in Abbreviations: AB, antibody; CK18, cytokeratin 18; COX IV, mitochondrial Complex vestibular nerve. ′ IV; DAPI, (4 ,6-diamidino-2-phenylindole, dihydrochloride salt); Dcx, doublecortin; To investigate the UCP4 expression in different structures of the GFAP, glial fibrillar acidic protein; IHC, inner hair cells; MOD, modiolus; NF200, neurofilaments 200; OC, organ of Corti; OHC, outer hair cells; PB, phosphate buffer; PC, inner ear at the protein level and to examine its role in ROS pillar cells; PhC, phalangeal cells; PFA, paraformaldehyde; ROS, reactive oxygen species; regulation we now employ a well-established model of hypoxia SD, standard deviation; SEM, standard errors of mean; SG, spiral ganglion; SL, spiral (Gross et al., 2007). We compared the UCP4 expression in early limbus; SOD2, superoxide dismutase 2; SV, stria vascularis; VDAC, voltage dependent (postnatal day 2, P2), late postnatal (P5, P8, prior to the onset of anion channel; UCP, uncoupling protein; WB, Western blot. hearing) and adult (P28) rat cochlea to evaluate further hypotheses ⁎ Corresponding author at: Department of Physiology and Biophysics, University of Veterinary Medicine, 1210 Vienna, Austria. concerning the possible UCP4 participation in postnatal develop- E-mail address: [email protected] (E.E. Pohl). ment of the inner ear. 1044-7431/$ – see front matter © 2011 Published by Elsevier Inc. doi:10.1016/j.mcn.2011.03.002 A. Smorodchenko et al. / Molecular and Cellular Neuroscience 47 (2011) 244–253 245 Results spiral ganglion (SG, blue) and axons (black). WB analysis (Fig. 1B) shows that UCP4 is expressed as a band of approximately 36 kDa with Pattern of UCP4 distribution in the cochlea under physiological the highest level in OC, less in MOD. No UCP4 was detected in SV of P3 conditions rat cochlea. To obtain the pattern of protein distribution in different inner ear structures, we performed the immunohistochemistry of First, we have examined the cellular distribution of UCP4 in Wistar cryosections from P3 and P28 rats' cochleae. Fig. 1C (left panel) and rat cochlea using highly specific anti-UCP4 antibody (Smorodchenko Fig. S1 show the UCP4 immunoreactivity in OC, SG, SL and inner sulcus et al., 2009). The protein content in structures of newborn (postnatal cells of P3 animals. UCP4 is localized in mitochondria as confirmed by day 3, P3) and adult (postnatal day 28, P28) rats inner ear was a co-localization with mitochondrial porin VDAC (Fig. S1B). No UCP4 analyzed by WB and immunohistochemistry. was detected in SV (data not shown) and in SL of P28 rats Fig. 1C, right The schematic drawing (Fig. 1A) shows the cochlea emphasizing panel). Protein expression in cochleae of adult rats was mostly the structures on which we focused: spiral limbus (SL, gray), organ of restricted to spiral ganglion neurons and structures of OC (Fig. 1C, Corti (OC, pink), stria vascularis (SV, yellow), modiolus (MOD, green), right panel, Fig. 2A). The high-resolution image of newborn cochlea Fig. 1. UCP4 distribution in cochlea under physiological conditions. A. Schematic drawing shows the cochlea. SL-spiral limbus (gray), axons (black), MOD-modiolus (green), OC-organ of Corti (pink), SV-stria vascularis (yellow), SG-spiral ganglion (blue). B. Representative Western blot of lysates from freshly isolated organ of Corti (OC) with spiral limbus (SL), modiolus (MOD) and stria vascularis (SV) using anti-UCP4. Anti-actin and anti-VDAC antibodies were used as control for the sample loading and as mitochondria marker respectively. OC, MOD and SV were isolated from P3 rats. For each lane 20 μg protein were loaded. C. Confocal laser scanning microscopy image of OC, SL and SG of P3 rats (left panel) in comparison with P28 rats (right panel). Double-labeling with anti-UCP4 antibody (visualized by Alexa-488, green) and DAPI was performed on cryosections (20 μmthick).In P3 rat cochlea (left panel) UCP4 is homogenously distributed in different structures: SG neurons, SL, supporting cells and hair cells of OC (white arrows). In P28 rat cochlea (right panel) UCP4 is restricted to SG and OC cells. The complete images (left and right panels) are a result of a montage of two microscopical fields, taken under the same conditions. Scale bar, 40 μm. 246 A. Smorodchenko et al. / Molecular and Cellular Neuroscience 47 (2011) 244–253 demonstrated, that under physiological conditions, UCP4 immunore- UCP4 detection in hair cells activity is detected in mitochondria of outer (OHCs) and inner hair cells (IHCs) and, surprisingly, in mitochondria of supporting cells Data from literature (Mao et al., 1999) and from our previous study (inner phalangeal, Deiters' and pillar cells) (Fig. 2B). (Smorodchenko et al., 2009) showed that UCP4 mRNA and protein Fig. 2. UCP4 expression in supporting, outer and inner hair cells. A. Confocal laser scanning microscopy images of OC from freshly isolated rat cochlea (P28 rats). UCP4 in cytoplasm of OHCs and IHCs is stronger expressed than in inner phalangeal cell, PhC, (visualized by Alexa-488, green) and outer phalangeal cells (Deiters' cells, DC, arrowhead). Staining was performed on cryosections from freshly isolated cochlea (20 μm thick) and counterstained with DAPI (blue). PC, pilar cells. Scale bar, 50 μm. B. Merged confocal laser scanning microscopy image of OC (newborn, P3) shows the triple-labeling with anti-UCP4 (visualized by Alexa-488, green), anti-NF200 (visualized by Alexa-568, red) antibodies and DAPI (blue). Anti-UCP4 immunoreactivity is seen on the apical pole of all neurosensory hair cells and in the cytoplasm of supporting
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