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Expression Profiles of Two Types of Human Knee-Joint Cartilage

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Expression Profiles of Two Types of Human Knee-Joint Cartilage J Hum Genet (2003) 48:177–182 DOI 10.1007/s10038-003-0004-8 ORIGINAL ARTICLE Kensuke Ochi Æ Yataro Daigo Æ Toyomasa Katagiri Akihiko Saito-Hisaminato Æ Tatsuhiko Tsunoda Yoshiaki Toyama Æ Hideo Matsumoto Yusuke Nakamura Expression profiles of two types of human knee-joint cartilage Received: 16 December 2002 / Accepted: 27 December 2002 / Published online: 21 February 2003 Ó The Japan Society of Human Genetics and Springer-Verlag 2003 Abstract We have performed a comprehensive analysis Keywords Hyaline cartilage Æ Fibrocartilage Æ of gene-expression profiles in human articular cartilage Expression profiles Æ Marker gene Æ Regenerative (hyaline cartilage) and meniscus (fibrocartilage) by medicine means of a cDNA microarray consisting of 23,040 human genes. Comparing the profiles of the two types of cartilage with those of 29 other normal human tissues identified 24 genes that were specifically expressed in Introduction both cartilaginous tissues; these genes might be involved in maintaining phenotypes common to cartilage. We Several transcriptional factors are thought to be key also compared the cartilage profiles with gene expression factors directing differentiation of mesenchymal tissues: in human mesenchymal stem cells (hMSC), and detected molecules of the MYOD family for muscle differentiation 22 genes that were differentially expressed in cells rep- (Ferrari et al. 1998), PPARG2 for adipose tissue differ- resenting the two cartilaginous lineages, 11 specific to entiation (Rosen and Spiegelman 2000), and CBFA1 for each type, which could serve as markers for predicting osteogenic differentiation (Komori et al. 1997). Although the direction of chondrocyte differentiation. Our data SOX9 and CBFA1 are thought to be key transcriptional should also provide useful information about regenera- factors during cartilage differentiation (Bi et al. 1999), tion of cartilage, especially in support of efforts to other factors are likely to be involved as well (Takeda et al. identify cartilage-specific molecules as potential agents 2001). Articular cartilage (hyaline cartilage) of the knee, for therapeutic approaches to joint repair. and the knee meniscus (fibrocartilage), are different (Ross et al. 1995). Identification of common cis-elements in genes expressed specifically in these two types of cartilage K. Ochi Æ Y. Daigo Æ A. Saito-Hisaminato Æ Y. Nakamura (&) should yield insight into cartilage-specific transcriptional Laboratory of Molecular Medicine, regulation. Human Genome Center, Institute of Medical Science, Investigators interested in cartilage development and University of Tokyo, 4-6-1 Shirokanedai, regeneration have a few markers available for predicting Minato-ku, Tokyo 108-8639, Japan E-mail: [email protected] the direction of differentiation, i.e., type II collagen and Tel.: +81-3-5449-5372 aggrecan for hyaline cartilage, and type I collagen for Fax: +81-3-5449-5433 fibrocartilage (Burgeson et al. 1982; Ross et al. 1995; T. Katagiri Æ Y. Nakamura Carlberg et al. 2001). Cartilaginous cells are believed to Laboratory of Genome Technology, originate from multipotential mesenchymal cells that Human Genome Center, resemble human mesenchymal stem cells (hMSCs) Institute of Medical Science, (DeLise et al. 2000; Carlberg et al. 2001). Since hMSCs University of Tokyo, Tokyo, Japan are relatively easy to obtain, hMSC cultures are con- T. Tsunoda sidered to be good sources of cells for modeling regen- Laboratory for Medical Informatics, SNP Research Center, eration of mesenchymal tissues such as cartilage and Institute of Physical and Chemical Research (Riken), Kanagawa, Japan bone (Pittenger et al. 1999; Carlberg et al. 2001; Ochi et al. 2003). Thus, genes that are expressed specifically in K. Ochi Æ Y. Toyama Æ H. Matsumoto Department of Orthopaedic Surgery, either hyaline cartilage or fibrocartilage should be useful Keio University School of Medicine, markers to indicate the direction of differentiation. To Tokyo, Japan identify such genes, we have applied a cDNA microarray 178 containing 23,040 genes in a system that provides high- 2001). The intensity of each duplicated signal was evaluated throughput analysis of expression. In the work reported photometrically using the ArrayVision computer program (Imaging Research, Inc., St Catharines, Ontario, Canada). In- here, we evaluated the power of this system to detect tensities of the 29 individual normal tissues (test) and 29Mix cartilage-specific molecules. (control) were evaluated as described elsewhere (Saito-Hisaminato et al. 2002). The fluorescence intensities of Cy5 (test) and Cy3 (control) for each target spot were adjusted so that the mean Cy5/ Materials and methods Cy3 ratio of the 52 housekeeping genes was equal to one. We assigned a cut-off value to each microarray slide, using variance analysis. If both Cy3 and Cy5 signal intensities were less than the Clinical samples cut-off values, the expression level of the corresponding gene in that sample was assessed as low or absent. For other genes we All patients were diagnosed and treated by members of the calculated Cy5/Cy3 as a relative expression ratio. A two-dimen- Department of Orthopedic Surgery, Keio University School of sional hierarchical clustering method was performed as described Medicine. ‘‘Normal’’ articular cartilage samples were obtained before (Saito-Hisaminato et al. 2002). during total knee replacement surgery performed on eight female patients (age range 56–80 years, median 69 years) who were diag- nosed with primary osteoarthritis of the knee. In each case a non- affected site of articular cartilage, such as the patellar–femoral Semi-quantitative RT-PCR joint, was carefully peeled to provide samples for further investi- gations. ‘‘Normal’’ meniscus tissues were obtained from samples A3-lg aliquot of each RNA to be used for microarray analysis was removed during endoscopic meniscectomy of six patients (five male reverse-transcribed to single-stranded cDNA using oligo(dT)12–18 and one female; age range 13–28 years, median 20 years) who were primer and Superscript II (Invitrogen, Carlsbad, CA). Semi- diagnosed with traumatic meniscal injury; again, non-affected quantitative reverse transcription PCR (RT-PCR) was carried out tissue corresponding to each sample was obtained for our investi- for seven selected genes as described previously (Ono et al. 2000), gations. All 14 patients (or their families in some cases) gave using the following primer sets: for UBA52,5¢-GAT CTT TGT informed consent according to the guidelines of both Keio GAA GAC CCT CAC TG-3¢ and 5¢-CAG ATC ATC TTG TCG University and the University of Tokyo. Resected samples were CAG TTG TA-3¢; for RPL23,5¢-CTG TAT ATC ATC TCC GTG snap-frozen in liquid nitrogen immediately and sent to the Human AAG GG-3¢ and 5¢-AAG TCT GCA CAC TCC TTT GCT AC-3¢; Genome Center, Institute of Medical Science at the University of for RAB13,5¢-CAA CAA CAC TTA CAT CTC CAC CA-3¢ and Tokyo, without any personal identifiers. 5¢-GAG CAC TTG TTG GTG TTC TTC TT-3¢; for IGF2,5¢-CTT GGA CTT TGA ATC AAA TTG G-3¢ and 5¢-CCT CCT TTG GTC TTA CTG GG-3¢; for IGL@, 5¢-CAA CTG TAC ACC TAA AGG CTC TC-3¢ and 5¢-ATC TGA GAG GAG AGG AGA GTG Preparation, T7-based amplification, and labeling of RNAs A-3¢; for PDLIM1,5¢-CCA TAC AAG ATG AAT TTA GCC TCT G-3¢ and 5¢-GTC AGA CAC GTT ATA TT TGA TTG Total RNA was extracted from each frozen clinical sample and GG-3¢; and for COL1A1,5¢-CAT GTT CGG TTG GTC AAA from human mesenchymal stem cells (hMSC) purchased from GATA-3¢ and 5¢-AAT ACA AAA CCA CCA AGA CCT CC-3¢. BioWhittaker, Inc. (Walkersville, MD) to serve as a universal PCR reactions were optimized for the number of cycles to ensure control, using TRIzol reagent (Life Technologies, Inc., Rockville, product intensity within the linear phase of amplification. MD). Total RNAs of 29 normal human tissues (mesenteric adipose tissue, bone marrow, brain, heart, kidney, liver, lung, lymph node, mammary gland, pancreas, placenta, prostate, salivary gland, skeletal muscle, small intestine, spinal cord, spleen, stomach, testis, Results and discussion thymus, thyroid, trachea, uterus, colon, ovary, fetal brain, fetal kidney, fetal liver, and fetal lung) were obtained as described pre- viously (Saito-Hisaminato et al. 2002). Equal amounts of RNA Identification of genes that were highly expressed from each of the 29 normal tissues were pooled to serve as another in both hyaline cartilage and fibrocartilage universal control (29Mix). All RNA preparations were digested with RNase-free DNase I (Nippon Gene Co., Tokyo, Japan) ac- cording to the manufacturer’s recommendations. Two rounds of Comparison of expression profiles in cartilage with those T7-based RNA amplification and the preparation of cDNA probes of other normal human tissues should indicate genes were carried out as described elsewhere (Kitahara et al. 2001; Ochi that are preferentially expressed in cartilage. We selected et al. 2002). Amplified RNA (2.5 lg) from each cartilage sample 6707 genes for which data were present for hyaline (articular cartilage: a mixture of 8 cases; meniscus, 6 patients) was labeled with Cy5-dCTP (Amersham Biosciences, Uppsala, cartilage; 585 of them, including five collagen genes, Sweden); an equal amount of amplified RNA from each universal showed hyaline cartilage/29Mix ratios >10, and 209 control (29Mix or a pool of amplified RNA from hMSCs) was also showed hyaline cartilage/hMSC ratios >10 (data labeled with Cy3-dCTP (Amersham Biosciences) for hybridization not shown). Similarly, we selected 6436 genes for which to the cDNA microarray. data were present for fibrocartilage; 605 showed fibro- cartilage/29Mix ratios >10 and 145 showed fibrocarti- lage/hMSC ratios >10 (data not shown). Construction and analysis of the cDNA microarray Fabrication of our cDNA microarray slides has been described previously (Ono et al. 2000; Kitahara et al. 2001). Slides con- taining a duplicate set of 23,040 cDNA spots were used for each Identification of ‘‘cartilage-specific’’ genes analysis of expression profiles, to reduce experimental fluctuation.
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