The Japanese Society of Developmental Biologists

Develop. Growth Differ. (2015) 57, 200–208

doi: 10.1111/dgd.12194

Original Article

Periostin, a neurite outgrowth-promoting factor, is expressed at high levels in the primate cerebral cortex Eiji Matsunaga,* Sanae Nambu, Mariko Oka, Michio Tanaka, Miki Taoka and Atsushi Iriki Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute, Wako, Japan

Periostin (POSTN or osteoblast specific factor) is an extracellular matrix protein originally identified as a protein highly expressed in osteoblasts. Recently, periostin has been reported to function in axon regeneration and neuroprotection. In the present study, we focused on periostin function in cortical evolution. We performed a comparative gene expression analysis of periostin between rodents (mice) and primates (marmosets and macaques). Periostin was expressed at higher levels in the primate cerebral cortex compared to the mouse cerebral cortex. Furthermore, we performed overexpression experiments of periostin in vivo and in vitro. Periostin exhibited neurite outgrowth activity in cortical neurons. These results suggested the possibility that prolonged and increased periostin expression in the primate cerebral cortex enhances the cortical plasticity of the mammalian cerebral cortex. Key words: electroporation, macaque, marmoset, mouse, primary culture.

Introduction The cerebral cortex is an indispensable region for higher cognitive function, and it is highly diverse among various mammalian species. Primates (particularly humans) have a larger cerebral cortex than rodents. During embryogenesis, primate cortices have a more developed outer subventricular zone (OSVZ), which generates a greater number of neurons compared to rodent cortices (LaMonica et al. 2012; Geschwind & Rakic 2013). In addition, recent studies have shown that primate cerebral cortices differ in other aspects as well, such as complexity in the cortical areas, cytoarchitecture, and neural connections and increased white matter content (Krubitzer 2009; Yamamori 2011; Kaas 2012; Greig et al. 2013; Sun & Hevner 2014; Matsunaga et al. 2015). These differences in neurogenesis, brain size, and cellular differences of the neurons could contribute to cortical evolution and diversity among the mammalian species. Periostin (POSTN or osteoblast specific factor) is an extracellular glycoprotein originally identified as a molecule differentially expressed in osteoblasts and fibroblasts (Horiuchi et al. 1999). Then, the function in the

nervous system has been demonstrated from a biomedical perspective. It has been recently shown that periostin shows neurite outgrowth activity in cerebellar granule neuron (CGN) or dorsal root ganglion (DRG) neurons (Shih et al. 2014) and neuroprotective activity in adult cortical neurons (Shimamura et al. 2012). Previously, we performed a comprehensive gene expression analysis in Japanese macaques (Macaca fuscata) with tool-use training. We identified periostin as one of the genes with differential expression among individuals (Matsunaga et al., 2013). Thus, we suspected periostin to have some function in cognitive learning or the plasticity of surrounding cortical neurons by controlling cellular properties. It has been suggested that differential expressions of extracellular matrix proteins contribute to the cortical diversification among species (Nomura et al. 2008; Fietz et al. 2010; Higo et al. 2010; Stenzel et al. 2014). To explore the possibility that periostin is related to neural basis and species difference of cognitive ability, we performed a comparative gene expression analysis of periostin between rodents and primates. In addition, we conducted in vivo and in vitro functional analyses.

Materials and methods *Author to whom all correspondence should be addressed. Email: [email protected] Received 28 November 2014; revised 23 December 2014; accepted 23 December 2014. ª 2015 Japanese Society of Developmental Biologists

Ethics The research protocols were approved by the Animal Care and Use Committee of RIKEN, and they conformed

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to the National Institutes of Health Guide for the Care and Use of Laboratory Animals. Animals and sample preparation Pregnant mice (Mus musculus) were purchased from Japan SLC Inc. (Shizuoka, Japan) and bred in our laboratory facility or manipulated by in utero electroporation. We used three mice each from postnatal day 0 (P0) and P14, and four mice from postnatal 8 weeks (adulthood) for the histochemical analysis. We used four pregnant mice for the in utero electroporation. Common marmosets (Callithrix jacchus) were purchased from the Research Resource Center of RIKEN Institute. Neonatal marmosets were bred in the laboratory facility. We used two male and one female P0 marmosets and one male and two female adult marmosets (adults were >36 months old). The animals were maintained on a 12-h light-dark cycle at 27°C with 50% humidity. They had ad libitum access to water and a standard marmoset diet of CMS-1 (Clea Japan, Tokyo, Japan) with supplements. A 5.5-year-old male Japanese macaque (Macaca fuscata) was provided by the National BioResource Project. Before the experiment, the macaque was reared in a breeding facility at RIKEN and maintained on a 12-h light-dark cycle at 23°C–27°C with 60% humidity. The macaque had ad libitum access to water and a standard monkey chow (Clea Japan) with some fruit. The mice and marmosets were anesthetized with an intramuscular injection of sodium pentobarbital (150 and 75 mg/kg, respectively; Sumitomo Dainippon Pharma, Osaka, Japan). The macaque was anesthetized with an intravenous injection of sodium pentobarbital (75 mg/kg). All the animals were perfused with ice-cold phosphate-buffered saline (PBS, pH 7.4) or 0.1 M phosphate buffer (pH 7.4) solution and immediately dissected. The brains were embedded in a Tissue-Tek optimal cutting temperature (OCT) compound (Sakura Fine Technical, Tokyo, Japan) and frozen on dry ice. Frozen sections were cut serially at a thickness of 14–20 lm with a cryostat (Leica Microsystems GmbH, Wetzlar, Germany). Plasmid preparation The full length of the mouse periostin cDNA (Genbank No. AK030756) was obtained from FANTOM full-length cDNA clones (Carninci et al. 2005). An expression vector, pMiwIII-periostin-EGFP (enhanced green fluorescent protein), was obtained by inserting mouse periostin cDNA into the EcoRV site of the pMiwIII-EGFP expression vector (Matsunaga et al. 2006) with an In-Fusion HD Cloning Kit (Takara Bio, Otsu, Japan). In

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order to amplify the periostin cDNA and 15-bp extensions that were homologous to the vector sequence, we used the following primers: 5ʹ-GAGCTCGGTA CCGATATGGTTCCTCTCCTGCCC-3ʹ and 5ʹ-ATGGTT GTGGGGGATTGAGAACGGCCTTCTCTTG-3ʹ with KO D-Plus-Ver.2 DNA polymerase (TOYOBO, Tokyo, Japan). After cloning the vector, the amplifying DNA was confirmed by sequencing. In utero electroporation In utero electroporation was performed with a CUY-21 electroporator (BEX, Tokyo, Japan) and a LF650P5 tweezers-type electrode (BEX) as previously described (Tabata & Nakajima 2008). We injected the expression vectors into the lateral ventricles of mice embryos at embryonic day 14 (E14) with glass pipets and added four electric pulses at 35 mV for 50 ms with intervals of 950 ms. The embryos were collected 48 h after the electroporation. After fixation in PBS with 4% paraformaldehyde, the embryos were embedded in PBS with 20% sucrose solution, frozen, and cut serially at a thickness of 20 lm with a cryostat. Primary culture of rat hippocampal neurons We dissected the cortical region of E19 rat embryos and cultured the dissociated cells (5 9 104 cells per well) on 12-mm round glass coverslips (Thermo Fisher Scientific, Waltham, MA, USA) coated with poly-L-lysine (Sigma-Aldrich, St. Louis, MO, USA) in 24-well plates (BD Biosciences, San Jose, CA, USA). They were maintained in Neurobasal medium (Life Technologies, Grand Island, NY, USA) supplemented with B-27 (Life Technologies) and GlutaMAX (Life Technologies), as previously described (Noritake et al. 2009). For the analysis of neurite outgrowth, pMiwIII-EGFP (0.5 lg per well) expression vectors were transfected with lipofectamine 2000 (Life Technologies) on the third day in vitro (DIV3) in order to visualize neuronal morphology. At DIV5, the cells were fixed in PBS with 4% paraformaldehyde. After permeabilization in PBS with Triton-X100, transfected neurons were visualized clearly with a rabbit polyclonal anti-green fluorescent protein (GFP) antibody (1:500; Life Technologies) and an Alexa488-conjugated anti-rabbit IgG antibody (Life Technologies). ImageJ software with the NeuroJ plug-in (Meijering et al. 2004) was used to measure the length of the neurites. Cultured neurons were randomly selected for measurement of neurite length. For preparation of the conditioned media, pMiwIII-EGFP or pMiwIII-periostin-EGFP (1 lg) expression vectors were transfected into HEK293 cells in 6-well plates with lipofectamine 2000 (Life Technologies). One day after ª 2015 Japanese Society of Developmental Biologists

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transfection, HEK293 cells were incubated with Neurobasal/B-27/ GlutaMAX medium (Life Technologies) for 2 days, and the conditioned medium was collected and filtered with a 0.20-lm filter (Advantec, Saijyo, Japan). Western blot analyses were performed by the standard method with a rabbit polyclonal anti-GFP antibody (1:1000; Life Technologies), VECTASTAIN Universal Elite ABC kit (Vector Laboratories, Burlingame, CA, USA), and an ECL Western Blotting Detection System (GE Healthcare, Pittsburgh, PA, USA). Before the electrophoresis, we concentrated the conditioned medium with acetone and hydrochloric acid solution. We captured images with a LAS-3000 luminescent Image Analyzer (FUJIFILM Corporation, Tokyo, Japan). Histochemical analysis In situ hybridization was performed as previously described (Matsunaga et al. 2013). Commercially available full length of human periostin cDNA (BC106709) was used (Thermo Fisher Scientific). We used a probe synthesized from mouse periostin cDNA (AK030756) for the mouse sections and synthesized from human periostin cDNA for the marmoset or macaque sections. The homology of human periostin cDNA to marmoset (XM_003733104) or macaque (XM_001085814) was 94% or 97%, respectively. We detected a strong signal with the antisense probes; no signals were detected above background with the sense probes. The immunohistochemical analysis was performed as previously described (Matsunaga et al. 2011). The antibodies used were mouse monoclonal anti-ß-tubulin-III (1:200, TuJ1; SigmaAldrich LLC), or mouse monoclonal anti-NeuN (1:200; Merck Millipore, Billerica, MA, USA), or rabbit polyclonal anti-GFP (1:400; Life Technologies) and an Alexa488conjugated anti-rabbit IgG (1:200; Life Technologies) or Cy3-conjugated anti-mouse IgG (1:400; Jackson ImmunoResearch Laboratories, West Grove, PA, USA). All the images were captured with a NanoZoomer 2.0 slide scanner (Hamamatsu Photonics K.K., Hamamatsu, Japan) or a DP80 digital camera under a BX-53 microscope (Olympus Corporation, Tokyo, Japan). Adobe Photoshop software (ver. CS5; Adobe Systems, San Jose, CA, USA) was used to convert color images to black and white, crop unnecessary areas, and juxtapose panels or enhance the contrast and brightness, as required.

Results High-level periostin expression was transient in the mouse cerebral cortex First, we examined periostin expression in the mouse neocortex. In the embryonic stage, no clear expression ª 2015 Japanese Society of Developmental Biologists

was detected (data not shown), as previously reported (Zhu et al. 2008). Expression was first detected during the postnatal stage. At P0, only weak expression was seen in the neocortex (n = 3) (Fig. 1A–C). By P14, strong periostin-positive cells were seen throughout the neocortex (n = 3) (Fig. 1D– F). Most of the periostin-expressing cells were located in the deep layers (layer V and VI) of the neocortex. In contrast, there were few periostin-positive cells in the hippocampus (Fig. 1B, E, H, J). The number of periostin-positive cells transiently increased and decreased at the adult stage (n = 4) (Fig. 1G–J). In the adult stage, periostin showed regionally differential expressions. Periostin-positive cells were seen in the frontal and occipital cortex (Fig. 1G, I, J), whereas only a few cells were seen in the parietal cortex, including the primary somatosensory area (S1) (Fig. 1H, J). Periostin was more highly expressed in the primate cerebral cortex compared to the mouse cerebral cortex Next, we examined periostin expression in the primate brain. Strong periostin expression was seen throughout the marmoset neocortex at the neonatal stage (n = 3) (Fig. 2A–C), partly because marmosets are born in a more mature state compared to mice (Mashiko et al. 2012). In contrast to the mouse neocortex, periostin-expressing cells were seen not only in the deep layers (Layer V and VI) but also in the upper layers (layer II and III) of the neocortex. As in the mouse neocortex, the number of periostinexpressing cells decreased at the adult stage (n = 3) (Fig. 2D–F). However, expression was maintained in the adult parietal cortex (Fig. 2E), and periostinexpressing cells were seen in the upper layers of the neocortex (Fig. 2D–F). Periostin expression was also seen in the dentate gyrus of neonatal and adult marmoset brains (n = 3) (Fig. 2G, H). In the macaque brain, even at adulthood (5.5 years old, after sexual maturation), many periostin-positive cells were sparsely distributed from the layer II to VI in the S1 region (Fig. 2I). In order to determine the cell types of the periostinpositive cells, we performed immunostaining with NeuN, a marker for mature neurons. Immunohistochemical analysis revealed that periostin protein existed in the surface of neuronal cell body of the adult mouse neocortex (Shimamura et al. 2012). As previously reported, in situ hybridization and subsequent immunostaining revealed that periostin-positive cells were NeuN-positive neurons in the mouse and marmoset neocortices (n = 3) (Fig. 2J–M).

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Fig. 1. In situ hybridization for periostin in the frontal association (A, D, G), primary somatosensory (B, E, H), and primary visual area (C, F, I) of the developing mouse brain at postnatal day (P) 0 (P0; A–C), P14 (D–F), and at adulthood (G–J). Transverse section (A–I) and sagittal section (J). Note that periostin is transiently expressed during postnatal development, with most of the periostin-positive cells located in the deep layers of the neocortex. Particularly, in the S1 region, periostin-positive cells almost disappeared by adulthood, and no clear expression was seen in the hippocampus. Asterisk indicates fold of section (C). DG, dentate gyrus. FrA, frontal association area; Hp, hippocampus; M1, primary motor cortex; S1, primary somatosensory area; V1, primary visual area. Scale bars, 500 lm.

Periostin overexpression in the embryonic mouse brain expanded the ß-tubulin-positive intermediate zone Next, in order to examine periostin function in neocortical development, we performed overexpression experiments in embryonic mouse neocortex. We performed in utero electroporation of both the periostin- and EGFP-expression vectors or the EGFPexpression vector alone into E14 embryos and collected the embryos 48 h after electroporation. Immunostaining with antibodies against ß-tubulin and EGFP revealed that the ß-tubulin-positive intermediate zone (IZ) was expanded in the periostin-overexpressing area compared to the control area (n = 4/5) (Fig. 3A, B). Such an expansion was not seen in the EGFP-overexpressing embryos (n = 5/5). In order to confirm this effect more

precisely, we measured the relative ratio of the ß-tubulinpositive IZ to the whole neocortex and calculated the differences between the electroporated (periostin and EGFP or EGFP) and control areas (no vectors injected) (Fig. 3C). Although the EGFP-expressing vector exhibited no significant differences, the periostin-expressing vector increased the relative thickness of the IZ as compared to the control area (Fig. 3D). Periostin had neurite outgrowth activity in cortical dissociation culture neurons Next, in order to verify that the expansion of the IZ was caused by neurite outgrowth by postmitotic neurons in periostin-overexpressing areas, we performed dissociation culture experiments of embryonic rat neocortex. ª 2015 Japanese Society of Developmental Biologists

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Fig. 2. In situ hybridization for periostin in the prefrontal (A, D), primary somatosensory (S1; B, E, I), primary visual (C, F), and hippocampal area (G, H) of developing marmoset (A–H) and Rhesus macaque (I) at P0 (A–C, G) and adulthood (D–F, H, I). Note that periostin expression is also seen in the upper layers of the marmoset neocortex and in the dentate gyrus and that periostin-expressing cells are sparsely distributed in the neocortex of adult macaque. (J–M) In situ hybridization for periostin and subsequent immunostaining with NeuN in the mouse (J, K) and marmoset (L, M) S1 region. The arrowheads indicate periostin-expressing cells. Note that too much strong staining cells with periostin probes look NeuN-negative because strong NBT (nitro-blue tetrazolium chloride) /BCIP (5-Bromo-4Chloro-30 -Indolylphosphatase p-Toluidine salt) chromogenic stain of in situ hybridization quenches immunofluorescence. Scale bars = 500 lm (C, F, G, H, I) and 50 lm (K, M).

Three days after culturing with standard growth medium (DIV3), we incubated the cultured cortical neurons in conditioned medium derived from periostin-EGFP expression vector-transfected cells (Periostin-Sup) or control conditioned medium derived from EGFP expression vector-transfected cells (EGFP-Sup), and the effects on neurite outgrowth were analyzed. Two days after culture in conditioned medium (DIV5), the cultured neurons with Periostin-Sup and with EGFP-Sup extended long neurites, but the former neurons tended to grow more (Fig. 4A, B). Periostin-EGFP fusion protein was detected in the conditioned medium by western blot analysis (Fig. 4C), thus periostin protein seemed to extend neurites. To examine this more precisely, we measured the neurite length with NeuroJ software (Meijering et al. 2004). We counted 20 neurons with Periostin-Sup and 20 with EGFP-Sup from three independent culture experiments (n = 6–7 each). ª 2015 Japanese Society of Developmental Biologists

Although we found no significant differences in the length of the longest neurite per cell (Fig. 4D), we detected significant differences in the total length of the neurites per cell (Fig. 4E).

Discussion In this study, we performed comparative gene expression analysis and found that periostin was strongly expressed in the primate neocortex and hippocampus, even in adulthood, whereas the strong expression in the juvenile rodent brain was transient. Periostinexpressing cells were seen in the upper layer of the neocortex, which makes cortico-cortical connections, particularly evolved in the primate brain. These data suggested that prolonged and high levels of periostin expression in the primate cerebral cortex could be associated with primate-specific cortical properties.

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Fig. 3. Periostin overexpression increases the ß-tubulin-positive intermediate zone. The frontal area of mouse embryos at embryonic day (E) 16 (48 h after electroporation) on the experimental (A) and control side (B). The image of the control side (B) is horizontally inverted for easy comparison. The relative ratio (electroporated side/non-electroporated side) of the percentage of the ß-tubulinpositive IZ in the whole cortical layer (C, D). We measured the thickness of the IZ and the whole layer of the ß-tubulin-stained sections (C). The relative ratio of the intermediate zone is increased in case of co-electroporation of periostin and GFP-overexpression vectors compared to that with electroporation of the GFP-expression vector alone (D). The statistical analysis was done with a Mann–Whitney U-test (n = 4 each; we only used embryos highly electroporated). *P < 0.05. Exp, experimental (electroporated) side; Cont, control (non-electroporated) side. Scale bars, 50 lm (B) and 20 lm (C).

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By in vitro and in vivo overexpression experiments, we also demonstrated that periostin exhibited neurite outgrowth activity. Previously, it has been reported that periostin promotes neurite outgrowth in adult cortical neurons (Shimamura et al. 2012) and developing CGN or DRG neurons (Shih et al. 2014). Our results also support these in vitro studies. Thus, it seems that periostin increased neurite outgrowth in various types of neurons at various stages. The property may enhance axonal branch or synapse formation of afferent neurons in vivo. Further analysis is needed to explore the detailed mechanism, for example, cellular localization of periostin protein in axon, dendrites or synapse of the primate brain. In summary, periostin exhibited neurite outgrowth activity, and was expressed in higher levels in the primate than in the rodent cerebral cortex, particularly in adulthood. These findings suggest that the primate cortex might exhibit greater morphological plasticity than that of rodents, enabling the primate brain to change in accordance to the external environment or complex cognitive learning. Many molecules have been so far suggested as responsible factors for neocortical evolution and diversity by controlling transcriptional regulation, cell adhesion, axon guidance, signal transduction or synapse function (Ponting & Jackson 2005; Pollard et al. 2006; Watakabe et al. 2007; Johnson €var et al. 2010; et al. 2009; Takaji et al. 2009; Bilgu Higo et al. 2010; McLean et al. 2011; Hawrylycz et al. 2012; Li et al. 2012; Mashiko et al. 2012; Zeng et al. 2012; Hata et al. 2013; Bae et al. 2014; Matsunaga et al. 2014; Miller et al. 2014). In addition to these,

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Fig. 4. Analysis of periostin function in a dissociated culture. (A, B) A typical example of cortical neurons that were cultured in conditioned medium derived from EGFP expression vector-transfected HEK293 cells (A, EGFP-sup) and medium derived from periostin-EGFP expression vector-transfected HEK293 cells (B, Periostin-Sup). Western blot analysis of EGFP-Sup (left lane) and Periostin-Sup (right lane) with an anti-GFP antibody (C). Periostin-EGFP (approximately 117 kDa) was detected in the right lane. Note that the band is distorted because of the concentration of the culture medium (indicated with *). (D, E) Length of the longest neurite (D) and total length (E) of the neurites per cell of cortical neurons at 5 days in vitro (DIV) with EGFP-Sup or Periostin-Sup. The statistical analysis was done with a Student’s t-test (n = 20 each). **P < 0.01. Scale bar = 100 lm. ª 2015 Japanese Society of Developmental Biologists

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periostin seems to be a likely new candidate via enhancing neurite outgrowth activity of the surrounding neurons.

Acknowledgments We thank RIKEN RRC for DNA sequence analysis and the FANTOM Consortium Core Group for mouse cDNA clone and Dr Shigeyoshi Itohara for lab facility. The monkeys used in this study were provided by NBRP “Japanese Monkeys” through the National BioResource Project of the MEXT, Japan. This work was supported by JSPS KAKENHI Grant number 25750403 and Takeda Science Foundation (to E.M.), the JSPS through the “Funding Program for WorldLeading Innovative R&D on Science and Technology (FIRST Program),” initiated by the Council for Science and Technology Policy (CSTP) and the Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) by the MEXT of Japan (to A.I.).

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Periostin, a neurite outgrowth-promoting factor, is expressed at high levels in the primate cerebral cortex.

Periostin (POSTN or osteoblast specific factor) is an extracellular matrix protein originally identified as a protein highly expressed in osteoblasts...
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