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layers of articular cartilage line the bones of synovial joints and provide a smooth, wear-resistant structure that reduces friction and absorbs impact forces (Brandt et al. 1998). Loss or damage to articular cartilage is a hallmark of arthritic diseases and is one of the most common reasons that both young and old adults seek medical care. Millions of people are afflicted with arthritis, and it ultimately affects more than half of people over the age of 65 (Badley 1995; Yelin and Callahan 1995). A better understanding of the molecular mechanisms that create and maintain articular cartilage is crucial for discovering the causes of joint disorders and providing useful medical treatments.\nJoint formation begins during embryogenesis, when stripes of high cell density called interzones form across developing skeletal precursors (Haines 1947). Programmed cell death occurs within the interzone, and a three-layered interzone forms that has two layers of higher cell density flanking a region of lower cell density. Non-joint precursors of the skeleton typically develop into cartilage, which hypertrophies and is replaced by bone. However, cells within the high-density layers of the interzone are excluded from this process and develop into the permanent layers of articular cartilage found in the mature joint (Mitrovic 1978).\nStudies over the last 10 y have begun to elucidate some of the signaling pathways that contribute to the early stages of joint formation. Wnt14 is expressed in stripes at the sites where joints will form, and it is capable of inducing expression of other joint markers when misexpressed at new locations in the limb (Hartmann and Tabin 2001). Several members of the bone morphogenetic protein (BMP) family of secreted signaling molecules are also expressed in stripes at sites where joints will form, including those encoded by the genes Gdf5, Gdf6, Gdf7, Bmp2, and Bmp4 (Storm and Kingsley 1996; Wolfman et al. 1997; Francis-West et al. 1999; Settle et al. 2003). Of these, Gdf5 expression is most strikingly limited to regions where joints will develop and is one of the earliest known markers of joint formation. Mutations in either Gdf5 or the closely related Gdf6 gene also block formation of joints at specific locations, providing strong evidence that these molecules are essential for the joint formation process (Storm et al. 1994; Settle et al. 2003). However, mutations in Bmp2 or Bmp4 cause early embryonic lethality, making it difficult to test their role in joint formation (Winnier et al. 1995; Zhang and Bradley 1996).\nMuch less is known about how signaling pathways function during the subsequent maturation and maintenance of adult joint structures. Importantly, BMP signaling components are present in adult articular cartilage, suggesting that they may function during the late development or maintenance of this critical structure (Erlacher et al. 1998; Chubinskaya et al. 2000; Muehleman et al. 2002; Bau et al. 2002; Bobacz et al. 2003).\nBMPs bind tetrameric complexes of two type I and two type II transmembrane serine-threonine kinase receptors. Upon BMP binding, these complexes transduce a signal by phosphorylating members of the Smad family of transcription factors (Massague 1996). Recent experiments have implicated two different BMP type I receptors in skeletal patterning, BMPR1A and BMPR1B. Both receptors can bind BMP2, BMP4, and GDF5, although GDF5 shows higher affinity for BMPR1B (Koenig et al. 1994; ten Dijke et al. 1994; Yamaji et al. 1994; Nishitoh et al. 1996; Chalaux et al. 1998). Both receptors are also expressed in dynamic patterns during normal development. In limbs, Bmpr1a expression becomes restricted to joint interzones, perichondrium, periarticular cartilage, hypertrophic chondrocytes, and interdigital limb mesenchyme. In comparison, Bmpr1b expression is seen primarily in condensing precartilaginous mesenchymal cells, regions flanking joint interzones, perichondrium, and periarticular cartilage (Dewulf et al. 1995; Mishina et al. 1995; Zou et al. 1997; Baur et al. 2000). Null mutations in the Bmpr1b gene produce viable mice with defects in bone and joint formation that closely resemble those seen in mice missing Gdf5 (Storm and Kingsley 1996; Baur et al. 2000; Yi et al. 2000). Null mutations in Bmpr1a cause early embryonic lethality, with defects in gastrulation similar to those seen in mice with mutations in Bmp4 (Mishina et al. 1995; Winnier et al. 1995). Recent studies with floxed alleles suggest that Bmpr1a is also required for many later developmental events, but its roles in bone and joint formation have not yet been tested (Mishina 2003).\nA genetic system for activating or inactivating genes specifically in joint tissues would be particularly useful for further studies of joint formation and maintenance. Here we take advantage of the tissue-specific expression pattern of the Gdf5 gene to engineer a Cre/loxP system (Nagy 2000), Gdf5-Cre, that can be used to remove or ectopically express genes in joints. Tests with reporter mice show that this system is capable of modifying genes in all of the structures of the mature synovial joint, including the ligaments of the joint capsule, the synovial membrane, and the articular cartilage. Gdf5-Cre recombination bypasses the early embryonic lethality of null mutations in Bmpr1a, and shows that this receptor is required for early joint formation at some locations and for initiation of programmed cell death in webbing between digits. Interestingly, Bmpr1a is also required for postnatal maintenance of articular cartilage throughout most of the skeleton. In Gdf5-Cre/Bmpr1afloxP mice, articular cartilage initially forms normally, but subsequently loses expression of several key cartilage markers after birth. It ultimately fibrillates and degenerates, resulting in severe osteoarthritis and loss of mobility. These experiments suggest that BMP signaling is required for normal maintenance of postnatal articular cartilage, and that modulation of the BMP signaling pathway may play an important role in joint disease."}

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layers of articular cartilage line the bones of synovial joints and provide a smooth, wear-resistant structure that reduces friction and absorbs impact forces (Brandt et al. 1998). Loss or damage to articular cartilage is a hallmark of arthritic diseases and is one of the most common reasons that both young and old adults seek medical care. Millions of people are afflicted with arthritis, and it ultimately affects more than half of people over the age of 65 (Badley 1995; Yelin and Callahan 1995). A better understanding of the molecular mechanisms that create and maintain articular cartilage is crucial for discovering the causes of joint disorders and providing useful medical treatments.\nJoint formation begins during embryogenesis, when stripes of high cell density called interzones form across developing skeletal precursors (Haines 1947). Programmed cell death occurs within the interzone, and a three-layered interzone forms that has two layers of higher cell density flanking a region of lower cell density. Non-joint precursors of the skeleton typically develop into cartilage, which hypertrophies and is replaced by bone. However, cells within the high-density layers of the interzone are excluded from this process and develop into the permanent layers of articular cartilage found in the mature joint (Mitrovic 1978).\nStudies over the last 10 y have begun to elucidate some of the signaling pathways that contribute to the early stages of joint formation. Wnt14 is expressed in stripes at the sites where joints will form, and it is capable of inducing expression of other joint markers when misexpressed at new locations in the limb (Hartmann and Tabin 2001). Several members of the bone morphogenetic protein (BMP) family of secreted signaling molecules are also expressed in stripes at sites where joints will form, including those encoded by the genes Gdf5, Gdf6, Gdf7, Bmp2, and Bmp4 (Storm and Kingsley 1996; Wolfman et al. 1997; Francis-West et al. 1999; Settle et al. 2003). Of these, Gdf5 expression is most strikingly limited to regions where joints will develop and is one of the earliest known markers of joint formation. Mutations in either Gdf5 or the closely related Gdf6 gene also block formation of joints at specific locations, providing strong evidence that these molecules are essential for the joint formation process (Storm et al. 1994; Settle et al. 2003). However, mutations in Bmp2 or Bmp4 cause early embryonic lethality, making it difficult to test their role in joint formation (Winnier et al. 1995; Zhang and Bradley 1996).\nMuch less is known about how signaling pathways function during the subsequent maturation and maintenance of adult joint structures. Importantly, BMP signaling components are present in adult articular cartilage, suggesting that they may function during the late development or maintenance of this critical structure (Erlacher et al. 1998; Chubinskaya et al. 2000; Muehleman et al. 2002; Bau et al. 2002; Bobacz et al. 2003).\nBMPs bind tetrameric complexes of two type I and two type II transmembrane serine-threonine kinase receptors. Upon BMP binding, these complexes transduce a signal by phosphorylating members of the Smad family of transcription factors (Massague 1996). Recent experiments have implicated two different BMP type I receptors in skeletal patterning, BMPR1A and BMPR1B. Both receptors can bind BMP2, BMP4, and GDF5, although GDF5 shows higher affinity for BMPR1B (Koenig et al. 1994; ten Dijke et al. 1994; Yamaji et al. 1994; Nishitoh et al. 1996; Chalaux et al. 1998). Both receptors are also expressed in dynamic patterns during normal development. In limbs, Bmpr1a expression becomes restricted to joint interzones, perichondrium, periarticular cartilage, hypertrophic chondrocytes, and interdigital limb mesenchyme. In comparison, Bmpr1b expression is seen primarily in condensing precartilaginous mesenchymal cells, regions flanking joint interzones, perichondrium, and periarticular cartilage (Dewulf et al. 1995; Mishina et al. 1995; Zou et al. 1997; Baur et al. 2000). Null mutations in the Bmpr1b gene produce viable mice with defects in bone and joint formation that closely resemble those seen in mice missing Gdf5 (Storm and Kingsley 1996; Baur et al. 2000; Yi et al. 2000). Null mutations in Bmpr1a cause early embryonic lethality, with defects in gastrulation similar to those seen in mice with mutations in Bmp4 (Mishina et al. 1995; Winnier et al. 1995). Recent studies with floxed alleles suggest that Bmpr1a is also required for many later developmental events, but its roles in bone and joint formation have not yet been tested (Mishina 2003).\nA genetic system for activating or inactivating genes specifically in joint tissues would be particularly useful for further studies of joint formation and maintenance. Here we take advantage of the tissue-specific expression pattern of the Gdf5 gene to engineer a Cre/loxP system (Nagy 2000), Gdf5-Cre, that can be used to remove or ectopically express genes in joints. Tests with reporter mice show that this system is capable of modifying genes in all of the structures of the mature synovial joint, including the ligaments of the joint capsule, the synovial membrane, and the articular cartilage. Gdf5-Cre recombination bypasses the early embryonic lethality of null mutations in Bmpr1a, and shows that this receptor is required for early joint formation at some locations and for initiation of programmed cell death in webbing between digits. Interestingly, Bmpr1a is also required for postnatal maintenance of articular cartilage throughout most of the skeleton. In Gdf5-Cre/Bmpr1afloxP mice, articular cartilage initially forms normally, but subsequently loses expression of several key cartilage markers after birth. It ultimately fibrillates and degenerates, resulting in severe osteoarthritis and loss of mobility. These experiments suggest that BMP signaling is required for normal maintenance of postnatal articular cartilage, and that modulation of the BMP signaling pathway may play an important role in joint disease."}

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layers of articular cartilage line the bones of synovial joints and provide a smooth, wear-resistant structure that reduces friction and absorbs impact forces (Brandt et al. 1998). Loss or damage to articular cartilage is a hallmark of arthritic diseases and is one of the most common reasons that both young and old adults seek medical care. Millions of people are afflicted with arthritis, and it ultimately affects more than half of people over the age of 65 (Badley 1995; Yelin and Callahan 1995). A better understanding of the molecular mechanisms that create and maintain articular cartilage is crucial for discovering the causes of joint disorders and providing useful medical treatments.\nJoint formation begins during embryogenesis, when stripes of high cell density called interzones form across developing skeletal precursors (Haines 1947). Programmed cell death occurs within the interzone, and a three-layered interzone forms that has two layers of higher cell density flanking a region of lower cell density. Non-joint precursors of the skeleton typically develop into cartilage, which hypertrophies and is replaced by bone. However, cells within the high-density layers of the interzone are excluded from this process and develop into the permanent layers of articular cartilage found in the mature joint (Mitrovic 1978).\nStudies over the last 10 y have begun to elucidate some of the signaling pathways that contribute to the early stages of joint formation. Wnt14 is expressed in stripes at the sites where joints will form, and it is capable of inducing expression of other joint markers when misexpressed at new locations in the limb (Hartmann and Tabin 2001). Several members of the bone morphogenetic protein (BMP) family of secreted signaling molecules are also expressed in stripes at sites where joints will form, including those encoded by the genes Gdf5, Gdf6, Gdf7, Bmp2, and Bmp4 (Storm and Kingsley 1996; Wolfman et al. 1997; Francis-West et al. 1999; Settle et al. 2003). Of these, Gdf5 expression is most strikingly limited to regions where joints will develop and is one of the earliest known markers of joint formation. Mutations in either Gdf5 or the closely related Gdf6 gene also block formation of joints at specific locations, providing strong evidence that these molecules are essential for the joint formation process (Storm et al. 1994; Settle et al. 2003). However, mutations in Bmp2 or Bmp4 cause early embryonic lethality, making it difficult to test their role in joint formation (Winnier et al. 1995; Zhang and Bradley 1996).\nMuch less is known about how signaling pathways function during the subsequent maturation and maintenance of adult joint structures. Importantly, BMP signaling components are present in adult articular cartilage, suggesting that they may function during the late development or maintenance of this critical structure (Erlacher et al. 1998; Chubinskaya et al. 2000; Muehleman et al. 2002; Bau et al. 2002; Bobacz et al. 2003).\nBMPs bind tetrameric complexes of two type I and two type II transmembrane serine-threonine kinase receptors. Upon BMP binding, these complexes transduce a signal by phosphorylating members of the Smad family of transcription factors (Massague 1996). Recent experiments have implicated two different BMP type I receptors in skeletal patterning, BMPR1A and BMPR1B. Both receptors can bind BMP2, BMP4, and GDF5, although GDF5 shows higher affinity for BMPR1B (Koenig et al. 1994; ten Dijke et al. 1994; Yamaji et al. 1994; Nishitoh et al. 1996; Chalaux et al. 1998). Both receptors are also expressed in dynamic patterns during normal development. In limbs, Bmpr1a expression becomes restricted to joint interzones, perichondrium, periarticular cartilage, hypertrophic chondrocytes, and interdigital limb mesenchyme. In comparison, Bmpr1b expression is seen primarily in condensing precartilaginous mesenchymal cells, regions flanking joint interzones, perichondrium, and periarticular cartilage (Dewulf et al. 1995; Mishina et al. 1995; Zou et al. 1997; Baur et al. 2000). Null mutations in the Bmpr1b gene produce viable mice with defects in bone and joint formation that closely resemble those seen in mice missing Gdf5 (Storm and Kingsley 1996; Baur et al. 2000; Yi et al. 2000). Null mutations in Bmpr1a cause early embryonic lethality, with defects in gastrulation similar to those seen in mice with mutations in Bmp4 (Mishina et al. 1995; Winnier et al. 1995). Recent studies with floxed alleles suggest that Bmpr1a is also required for many later developmental events, but its roles in bone and joint formation have not yet been tested (Mishina 2003).\nA genetic system for activating or inactivating genes specifically in joint tissues would be particularly useful for further studies of joint formation and maintenance. Here we take advantage of the tissue-specific expression pattern of the Gdf5 gene to engineer a Cre/loxP system (Nagy 2000), Gdf5-Cre, that can be used to remove or ectopically express genes in joints. Tests with reporter mice show that this system is capable of modifying genes in all of the structures of the mature synovial joint, including the ligaments of the joint capsule, the synovial membrane, and the articular cartilage. Gdf5-Cre recombination bypasses the early embryonic lethality of null mutations in Bmpr1a, and shows that this receptor is required for early joint formation at some locations and for initiation of programmed cell death in webbing between digits. Interestingly, Bmpr1a is also required for postnatal maintenance of articular cartilage throughout most of the skeleton. In Gdf5-Cre/Bmpr1afloxP mice, articular cartilage initially forms normally, but subsequently loses expression of several key cartilage markers after birth. It ultimately fibrillates and degenerates, resulting in severe osteoarthritis and loss of mobility. These experiments suggest that BMP signaling is required for normal maintenance of postnatal articular cartilage, and that modulation of the BMP signaling pathway may play an important role in joint disease."}

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layers of articular cartilage line the bones of synovial joints and provide a smooth, wear-resistant structure that reduces friction and absorbs impact forces (Brandt et al. 1998). Loss or damage to articular cartilage is a hallmark of arthritic diseases and is one of the most common reasons that both young and old adults seek medical care. Millions of people are afflicted with arthritis, and it ultimately affects more than half of people over the age of 65 (Badley 1995; Yelin and Callahan 1995). A better understanding of the molecular mechanisms that create and maintain articular cartilage is crucial for discovering the causes of joint disorders and providing useful medical treatments.\nJoint formation begins during embryogenesis, when stripes of high cell density called interzones form across developing skeletal precursors (Haines 1947). Programmed cell death occurs within the interzone, and a three-layered interzone forms that has two layers of higher cell density flanking a region of lower cell density. Non-joint precursors of the skeleton typically develop into cartilage, which hypertrophies and is replaced by bone. However, cells within the high-density layers of the interzone are excluded from this process and develop into the permanent layers of articular cartilage found in the mature joint (Mitrovic 1978).\nStudies over the last 10 y have begun to elucidate some of the signaling pathways that contribute to the early stages of joint formation. Wnt14 is expressed in stripes at the sites where joints will form, and it is capable of inducing expression of other joint markers when misexpressed at new locations in the limb (Hartmann and Tabin 2001). Several members of the bone morphogenetic protein (BMP) family of secreted signaling molecules are also expressed in stripes at sites where joints will form, including those encoded by the genes Gdf5, Gdf6, Gdf7, Bmp2, and Bmp4 (Storm and Kingsley 1996; Wolfman et al. 1997; Francis-West et al. 1999; Settle et al. 2003). Of these, Gdf5 expression is most strikingly limited to regions where joints will develop and is one of the earliest known markers of joint formation. Mutations in either Gdf5 or the closely related Gdf6 gene also block formation of joints at specific locations, providing strong evidence that these molecules are essential for the joint formation process (Storm et al. 1994; Settle et al. 2003). However, mutations in Bmp2 or Bmp4 cause early embryonic lethality, making it difficult to test their role in joint formation (Winnier et al. 1995; Zhang and Bradley 1996).\nMuch less is known about how signaling pathways function during the subsequent maturation and maintenance of adult joint structures. Importantly, BMP signaling components are present in adult articular cartilage, suggesting that they may function during the late development or maintenance of this critical structure (Erlacher et al. 1998; Chubinskaya et al. 2000; Muehleman et al. 2002; Bau et al. 2002; Bobacz et al. 2003).\nBMPs bind tetrameric complexes of two type I and two type II transmembrane serine-threonine kinase receptors. Upon BMP binding, these complexes transduce a signal by phosphorylating members of the Smad family of transcription factors (Massague 1996). Recent experiments have implicated two different BMP type I receptors in skeletal patterning, BMPR1A and BMPR1B. Both receptors can bind BMP2, BMP4, and GDF5, although GDF5 shows higher affinity for BMPR1B (Koenig et al. 1994; ten Dijke et al. 1994; Yamaji et al. 1994; Nishitoh et al. 1996; Chalaux et al. 1998). Both receptors are also expressed in dynamic patterns during normal development. In limbs, Bmpr1a expression becomes restricted to joint interzones, perichondrium, periarticular cartilage, hypertrophic chondrocytes, and interdigital limb mesenchyme. In comparison, Bmpr1b expression is seen primarily in condensing precartilaginous mesenchymal cells, regions flanking joint interzones, perichondrium, and periarticular cartilage (Dewulf et al. 1995; Mishina et al. 1995; Zou et al. 1997; Baur et al. 2000). Null mutations in the Bmpr1b gene produce viable mice with defects in bone and joint formation that closely resemble those seen in mice missing Gdf5 (Storm and Kingsley 1996; Baur et al. 2000; Yi et al. 2000). Null mutations in Bmpr1a cause early embryonic lethality, with defects in gastrulation similar to those seen in mice with mutations in Bmp4 (Mishina et al. 1995; Winnier et al. 1995). Recent studies with floxed alleles suggest that Bmpr1a is also required for many later developmental events, but its roles in bone and joint formation have not yet been tested (Mishina 2003).\nA genetic system for activating or inactivating genes specifically in joint tissues would be particularly useful for further studies of joint formation and maintenance. Here we take advantage of the tissue-specific expression pattern of the Gdf5 gene to engineer a Cre/loxP system (Nagy 2000), Gdf5-Cre, that can be used to remove or ectopically express genes in joints. Tests with reporter mice show that this system is capable of modifying genes in all of the structures of the mature synovial joint, including the ligaments of the joint capsule, the synovial membrane, and the articular cartilage. Gdf5-Cre recombination bypasses the early embryonic lethality of null mutations in Bmpr1a, and shows that this receptor is required for early joint formation at some locations and for initiation of programmed cell death in webbing between digits. Interestingly, Bmpr1a is also required for postnatal maintenance of articular cartilage throughout most of the skeleton. In Gdf5-Cre/Bmpr1afloxP mice, articular cartilage initially forms normally, but subsequently loses expression of several key cartilage markers after birth. It ultimately fibrillates and degenerates, resulting in severe osteoarthritis and loss of mobility. These experiments suggest that BMP signaling is required for normal maintenance of postnatal articular cartilage, and that modulation of the BMP signaling pathway may play an important role in joint disease."}