Microarray analysis of gene expression patterns during healing of rat corneas after excimer laser photorefractive keratectomy.

PURPOSE To characterize changes over time in the genomic expression profile of rat corneas after excimer laser photorefractive keratectomy (PRK), in an effort to better understand the cellular response to injury and the dynamic changes that occur in gene expression patterns as a wound heals. METHODS The corneal gene expression profile of 1176 genes at 3 and 7 days after PRK was determined and compared with untreated corneal gene expression patterns by interrogating commercially available cDNA arrays with labeled target cDNA prepared from pooled total RNA harvested from the respective treatment group of adult male rats. The gene expression patterns were inferred based on the hybridization intensities of the probes on the cDNA arrays. The hybridization signals were globally normalized and filtered. The data were analyzed by using hierarchical and k-means clustering algorithms before and after normalization of variances. RESULTS Of the 1176 cDNA elements on the array, 588 consistently produced similar results in replicate experiments and comprised the data set analyzed in this work. In total, 73 genes were identified, with expression levels that differed by at least threefold at either 3 or 7 days after PRK. At 3 days after PRK, 70 genes were identified with expression levels that differed by more than threefold, compared with the expression level in untreated animals. The expression of 42 genes increased by threefold or more, whereas expression of 28 genes decreased by threefold or more. By day 7 after PRK, the number of genes displaying more than a threefold difference in expression pattern was reduced to 27 genes, 20 of which showed elevated levels, whereas 7 exhibited decreased levels. Hierarchical clustering of the 588 studied genes produced 10 clusters with correlation coefficients of 0.9 or greater. To determine whether any of the clusters were overrepresented by genes with related functions, the cumulative hypergeometric probability was calculated by obtaining the observed number of functionally related genes within each of the 10 clusters. Seven of the clusters were statistically overrepresented by one or more categories of functionally related genes, such as cell cycle regulators, transcription factors, and metabolic pathway genes. Clustering analysis of 56 genes generally considered to influence corneal wound healing produced 10 gene clusters with correlation coefficients of at least 0.9. Expression of 23 of these 56 genes increased at day 3, then decreased at day 7 to levels similar to those on day 0. These included several growth factors (VEGF, FGF, IGF-I), proteases (PAI-1, PAI-2A) and protease inhibitors (TIMP-2 and TIMP-3). Expression of nine genes increased on both days 3 and 7 compared with expression on day 0 (e.g., TGFB1, TGFBIIR, M6P/IGFR-2), and no genes decreased on both days 3 and 7, compared with day 0. CONCLUSIONS Microarray analysis of 1176 identified 588 genes with reproducible patterns of expression in rat corneas on days 3 and 7 after PRK and 73 genes with a threefold change in expression compared with untreated corneas. Hierarchical clustering of these 588 genes identified 10 clusters of genes with very similar patterns of expression. Clustering of genes with similar patterns of expression implies a common regulatory pathway for the genes within a cluster, and identifies potential new targets for regulating corneal wound healing.

[1]  G. Borah,et al.  Cytokines, growth factors, and plastic surgery. , 2001, Plastic and reconstructive surgery.

[2]  M. Goebeler,et al.  Chemokines in cutaneous wound healing , 2001, Journal of leukocyte biology.

[3]  R. Beuerman,et al.  Differential expression of glyceraldehyde-3-phosphate dehydrogenase (GAPDH), ß actin and hypoxanthine phosphoribosyltransferase (HPRT) in postnatal rabbit sclera , 2001, Current eye research.

[4]  J. Rowsey,et al.  Measurement of mRNAs for TGFss and extracellular matrix proteins in corneas of rats after PRK. , 2000, Investigative ophthalmology & visual science.

[5]  E. Brown,et al.  Genomic analysis of gene expression in C. elegans. , 2000, Science.

[6]  D. Azar,et al.  Differential expression of MT1-MMP (MMP-14) and collagenase III (MMP-13) genes in normal and wounded rat corneas. , 2000, Investigative ophthalmology & visual science.

[7]  Henry V. Baker,et al.  Understanding the Growth Phenotype of the Yeastgcr1 Mutant in Terms of Global Genomic Expression Patterns , 2000, Journal of bacteriology.

[8]  Christian A. Rees,et al.  Molecular portraits of human breast tumours , 2000, Nature.

[9]  A. Rizzino,et al.  DNA microarray analyses of genes regulated during the differentiation of embryonic stem cells , 2000, Molecular reproduction and development.

[10]  A. Hutcheon,et al.  Activation of epidermal growth factor receptor during corneal epithelial migration. , 2000, Investigative ophthalmology & visual science.

[11]  E. Lander,et al.  Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Ash A. Alizadeh,et al.  Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling , 2000, Nature.

[13]  C. Sotozono,et al.  Growth factors: importance in wound healing and maintenance of transparency of the cornea , 2000, Progress in Retinal and Eye Research.

[14]  G. Church,et al.  Systematic determination of genetic network architecture , 1999, Nature Genetics.

[15]  G. van den Engh,et al.  Characterization of differentially expressed genes in purified Drosophila follicle cells: toward a general strategy for cell type-specific developmental analysis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[16]  A. Hanyu,et al.  Functional difference of TGF-beta isoforms regulating corneal wound healing after excimer laser keratectomy. , 1999, Experimental eye research.

[17]  R. Mohan,et al.  Expression of HGF, KGF, EGF and receptor messenger RNAs following corneal epithelial wounding. , 1999, Experimental eye research.

[18]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  C. Chan,et al.  Inflammatory response in the early stages of wound healing after excimer laser keratectomy. , 1998, Archives of ophthalmology.

[20]  A. Nesburn,et al.  Extracellular matrix changes in human corneas after radial keratotomy. , 1998, Experimental eye research.

[21]  S. Jain,et al.  Gelatinase B and A expression after laser in situ keratomileusis and photorefractive keratectomy. , 1998, Archives of ophthalmology.

[22]  W T Lawrence,et al.  Physiology of the acute wound. , 1998, Clinics in plastic surgery.

[23]  D. Azar,et al.  Expression of gelatinases A and B, and TIMPs 1 and 2 during corneal wound healing. , 1998, Investigative ophthalmology & visual science.

[24]  A. Hanyu,et al.  Expression of transforming growth factor β superfamily and their receptors in the corneal stromal wound healing process after excimer laser keratectomy , 1998, The British journal of ophthalmology.

[25]  M. Fini,et al.  Regulation of paracrine cytokine balance controlling collagenase synthesis by corneal cells. , 1997, Investigative ophthalmology & visual science.

[26]  S. Jain,et al.  Matrix Metalloproteinases Are Expressed During Wound Healing After Excimer Laser Keratectomy , 1996, Cornea.

[27]  L. Wheeler,et al.  Effect of platelet‐derived growth factor on rabbit corneal wound healing , 1995, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[28]  H. Steenfos,et al.  Growth factors and wound healing. , 1994, Scandinavian journal of plastic and reconstructive surgery and hand surgery.

[29]  G. Schultz,et al.  Growth factors and wound healing: Part II. Role in normal and chronic wound healing. , 1993, American journal of surgery.

[30]  G. Schultz,et al.  Growth factors and wound healing: biochemical properties of growth factors and their receptors. , 1993, American journal of surgery.

[31]  P. Khaw,et al.  Detection of transforming growth factor-alpha messenger RNA and protein in human corneal epithelial cells. , 1992, Investigative ophthalmology & visual science.

[32]  P. Khaw,et al.  EFFECTS OF GROWTH FACTORS ON CORNEAL WOUND HEALING , 1992, Acta ophthalmologica. Supplement.

[33]  A. Tarkkanen,et al.  Epidermal growth factor in human tear fluid: A minireview , 1991, International Ophthalmology.

[34]  G. Waring,et al.  Healing of excimer laser ablated monkey corneas. An immunohistochemical evaluation. , 1990, Archives of ophthalmology.

[35]  D. Botstein,et al.  The transcriptional program in the response of human fibroblasts to serum. , 1999, Science.

[36]  D. Azar,et al.  Immunolocalization and gene expression of matrilysin during corneal wound healing. , 1999, Investigative Ophthalmology and Visual Science.

[37]  T. Tervo,et al.  Release of TGF-beta 1 and VEGF in tears following photorefractive keratectomy. , 1997, Current eye research.

[38]  S. O'Kane,et al.  Transforming growth factor βs and wound healing , 1997 .

[39]  C. Sotozono,et al.  High total TGF-beta 2 levels in normal human tears. , 1996, Current eye research.

[40]  C. Sotozono,et al.  High total TGF-β2 levels in normal human tears , 1996 .

[41]  C. Foster,et al.  Expression of collagens I, III, IV and V mRNA in excimer wounded rat cornea: analysis by semi-quantitative PCR. , 1995, Current eye research.

[42]  A. Tarkkanen,et al.  Plasmin and plasminogen activator activities in tear fluid during corneal wound healing after anterior keratectomy. , 1989, Current eye research.