Distinct Roles Of CCN1 And CCN2 In Limb Development
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1 Distinct Roles Of CCN1 And CCN2 In Limb Development Jie Jiang, PhD 1, Jessica Ong, BS 1, Faith Hall-Glenn, PhD 2, Teni Anbarchian, BS 1, Karen M. Lyons, PhD 1. 1 University of California, Los Angeles, Los Angeles, CA, USA, 2 University of California, San Francisco, San Francisco, CA, USA. Disclosures: J. Jiang: None. J. Ong: None. F. Hall-Glenn: None. T. Anbarchian: None. K.M. Lyons: None. Introduction: The CCN family of matricellular proteins is essential for many aspects of development, including skeletal development. While CCN1 and CCN2 are two of the most well-studied CCN family members, many questions remain about their roles in limb development. CCN1 and CCN2 mrna and protein expression are very similar within the developing limb, and it has been hypothesized they play similar roles during endochondral bone formation based on similar activities in vitro. Our previous studies have shown that deletion of CCN2 in chondrocytes resulted in perinatal lethality due to improper development of the ribs. These mice exhibit a range of skeletal defects including craniofacial abnormalities, sternal misalignment, kinked ribs, and deformed limbs. However, the function of Ccn1 in developing limbs has not been explored. In this study, we will examine the skeletal phenotypes in CCN1, CCN2, and CCN1/CCN2 cartilage specific (Col2Cre) conditional knockout mice during limb development to determine the shared and unique functions of these proteins. Methods: CCN2 floxed mice were generated previously in our laboratory, and CCN1 floxed mice were a gift from Dr. Lester Lau. To generate cartilage-specific deletion of CCN1 and CCN2, floxed mice were mated to Col2a1-Cre mice. Embryos were harvested at E16.5 and P0 and their skeletal phenotypes were examined. E16.5 embryos were paraffin embedded and sectioned for histological analysis. P0 embryos were processed for whole mount skeletal preparation. Results: Previously, we presented at the ORS that CCN1+CCN2 double mutants (DM) showed a more severe chondrodysplasia phenotype as compared to CCN2 mutants. This result led us to hypothesize that CCN1 and CCN2 have redundant roles during development. The previous studies were performed using a conditional allele of CCN1 that exhibited hypomorphic activity in all cells. Here, we use a conditional CCN1 allele that exhibits no hypomorphic activity in the absence of Cre. The analysis shown here (Fig. 1) revealed that CCN1 mutants had a very subtle skeletal phenotype, and that CCN2 plays a much more dominant role, as the DM phenotype resembles that of a CCN2 knockout. Under close examination of CCN1 mutants, we found several abnormalities in the axial skeleton, including an enlarged foramen magnum and an enlarged C1 vertebra (Fig. 1B). When examining the appendicular skeleton (Fig. 1C), we found that the CCN1 mutant had a normal phenotype. As previously mentioned, the CCN2 mutant showed a wide range of skeletal defects in both the axial and appendicular skeleton, including malformation in the spine, ribs, and limbs. DM resembles the CCN2 knockout with a slight increase in the severity of the malformation, especially in axial elements, which suggest that CCN1 and CCN2 may have more overlapping roles within the axial skeleton as compared to the appendicular skeleton.
2 The absence of a more severe phenotype in appendicular elements in the DM was unexpected based on the known functions of CCN1 and CCN2 during chondrogenesis in vitro and their expression in the appendicular skeleton in vivo. Histological analysis of E16.5 growth plate (Fig. 2) showed that the CCN1 mutant had a larger reserve zone, while both CCN2 and DM had smaller reserve zones compared to WT mice. CCN1 mutants had normal proliferative and hypertrophic zones while both CCN2 and DM had smaller proliferative and larger hypertrophic zones as compared to WT mice. Although DM and CCN2 growth plates are similar, DM mice did demonstrate longer hypertrophic zones compared with CCN2 mutants.
3 To further examine the effects of CCN1 and CCN2 on limb development, we examined their effect on chondrocyte proliferation and apoptosis. Tunnel staining showed no difference in apoptosis between CCN1, CCN2, and DM compared to WT mice at E16.6. We used phosphorylated-histoneh3, a sensitive marker for cells in the S phase, to quantify cell proliferation (Fig. 3). We found that CCN1 mutant mice exhibited a slight increase in the number of proliferating cells in both the reserve and proliferating zones compared to WT mice. CCN2 mutants, on the other hand, exhibited a significant decrease in proliferation in both the reserve and proliferating zones compared to WT mice. Interestingly, DM showed an intermediate phenotype, with slightly more proliferating cells in the reserve zone compared to CCN2 mutants, but still significantly less proliferation compared to WT and CCN1 mutant mice. In the proliferative zone, DM had a significantly higher number of proliferating cells compared to CCN2 mutants, but this was still significantly lower compared to CCN1 mutant and WT mice.
4 Discussion: Our results show that CCN2 plays a more dominant role in chondrogenesis than does CCN1, in spite of robust overlapping expression of both genes in cartilage. CCN1 and CCN2 do have some overlapping functions, particularly within the axial skeleton. However, they have distinct, opposing functions in the developing limb despite their similar expression patterns: within the appendicular skeleton, DM resulted in an unexpected correction of the proliferative defect seen in CCN2 knockout
5 mice. The majority of studies have shown that CCN1 and CCN2 have similar functions in vitro and in vivo. For example, both CCN1 and CCN2 induce osteogenesis and promote angiogenesis in vitro and/or in vivo. On the other hand CCN1 and CCN2 exhibit opposite effects during fibrosis; CCN1 induces fibroblast senescence and reduces scarring while CCN2 promotes fibrosis by stimulating cell proliferation and matrix deposition. We speculate that the rescue of the proliferative defect in the DM as compared to CCN2 mutant may be attributed to the differential role of CCN1 in promoting cell senescence. The exacerbated phenotype in the hypertrophic zone of the DM is likely due to the similar function of CCN1 and CCN2 s in promoting angiogenesis through regulation of Vegf expression in hypertrophic chondrocytes. Further studies in vivo and in vitro are in progress to test these possibilities. Significance: Osteoarthritis (OA) is one of the leading cause of disability in the US. There is an urgent need for effective therapies due to the limitations of current treatment. Changes in extracellular matrix (ECM) composition plays a central role in OA. Thus understanding the mechanism by which the ECM is elaborated and maintained is essential for the development of effective therapies. Member of the CCN family of matricellular proteins regulate chondrocyte survival, differentiation and ECM production, suggesting they may be highly effective therapeutic targets. In this study we examine the function of CCN1 and CCN2 in cartilage development using genetically modified murine models. Acknowledgments: The project is supported by NIAMS of NIH under the award number R01AR We would also like to acknowledge Dr. Lau for providing us with Ccn1 flox mice. References: N/A ORS 2014 Annual Meeting Poster No: 0539
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