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Scientific Article   |    
Prevention of Chondrocyte Apoptosis
Darryl D. D'Lima, MD; Sanshiro Hashimoto, MD; Peter C. Chen, PhD; Martin K. Lotz, MD; Clifford W. ColwellJr., MD
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Darryl D. D’Lima, MD
Peter C. Chen, PhD
Clifford W. Colwell Jr., MD
Division of Orthopaedic Surgery, Scripps Clinic, MS126, 11025 North Torrey Pines Road, Suite 140, La Jolla, CA 92037. E-mail address for D.D. D’Lima: ddlima@scripps.edu. E-mail address for C.W. Colwell Jr.: colwell@scripps.edu

Sanshiro Hashimoto, MD
Martin K. Lotz, MD
Division of Arthritis Research, The Scripps Research Institute, MEM 161, 10550 North Torrey Pines Road, La Jolla, CA 92037

In support of their research or preparation of this manuscript, one or more of the authors received grants or outside funding from Orthopaedic Research and Education Foundation Grant 98-052, National Institutes of Health Grant AG07996, the ALSAM Foundation, and the Skaggs Institute for Research. None of the authors received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

The Journal of Bone & Joint Surgery.  2001; 83:S25-26 
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The occurrence of chondrocyte apoptosis may be cri­tical in determining the extent of a lesion and sub­sequent repair after mechanical injury to articular cartilage. Agents that prevent apoptosis and increase chondrocyte survival may prove beneficial in the treatment of these ­lesions. This set of experiments was designed to determine the efficacy of some known apoptosis inhibitors in preventing chon­drocyte apoptosis after mechanical injury.
 
 
In the first set of experiments, thirty full-thickness cartilage explants, 5 mm in diameter, were harvested from the weight-bearing regions of the medial femoral condyle of three fresh bovine joints with use of a dermal punch. Explants were cultured for forty-eight hours in Dulbecco modified Eagle medium supplemented with 10% fetal bovine serum. Explants were divided into three groups: control, loaded, and loaded + CI. The loaded group was subjected to a radially unconfined single static load of 23 MPa for 500 msec and recultured in fresh media for forty-eight hours postinjury. The loaded + CI group underwent the same loading, but the specimens were cultured in fresh media containing 100 mM of the caspase ­inhibitor z-VAD.fmk. The control group did not undergo loading. In a second set of experiments, forty-eight bovine cartilage explants were divided into four groups: control, loaded, loaded + D, and loaded + I. The loaded, loaded + D, and loaded + I groups were loaded as described above. The loaded + D explants were cultured in media containing 0.1 mM dexa­methasone, and the loaded + I explants were cultured in media containing 50 ng/mL IGF-1 (insulin-like growth factor-1). In a third set of experiments, thirty explants were harvested from macroscopically normal fresh human cadaver tibial ar­ticular cartilage and were divided into control, loaded, and loaded + CI groups. Both loaded groups were loaded at 23 MPa, and the loaded + CI group was cultured in media containing ­z-VAD.fmk. In a fourth set of experiments, explants were similarly harvested from macroscopically normal fresh human cadaver tibial articular cartilage and were divided into control, loaded, and loaded + I groups. Both loaded groups were subjected to 30% strain applied for 500 msec. Loaded + I explants were cultured in media containing 50 ng/mL IGF-1. Forty-eight hours after injury, the number of apoptotic cells in each explant was counted with use of TUNEL (terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling). Apoptosis was confirmed by electron microscopy in selected samples. For the first experiment, glycosaminoglycan levels in media were also measured, with use of dimethylene blue assay.
The levels of apoptotic cells in all of the loaded groups were significantly higher than those in the control groups (p < 0.001).
Caspase inhibition: Culturing loaded explants in z-VAD.fmk significantly reduced both the percentage of cells demonstrating apoptosis and the glycosaminoglycan levels in bovine and human explants (p < 0.01) (Figs. 1 and 2).
IGF-1: Both bovine and human explants demonstrated a decrease in apoptosis rates when cultured in media containing 50 ng/mL of IGF-1 (p < 0.05) (Fig. 1).
Dexamethasone: Loaded bovine explants demonstrated a decrease in apoptosis rates when cultured in media containing 0.1 mM dexamethasone (p < 0.05) (Fig. 1).
Glycosaminoglycan release: Compared with control bovine explants, loaded bovine explants demonstrated an increase in glycosaminoglycan levels in the media. This increase in glycosaminoglycan levels with loading was reduced by the ad­dition of z-VAD.fmk to the media after loading (p < 0.01) (Fig. 2).
We have previously shown that mechanical injury leads to chondrocyte apoptosis and that the percentage of cells undergoing apoptosis increases over time after injury1. This series of experiments was designed to determine whether certain agents could prevent this apoptosis. Apoptosis is mediated by a cascade of aspartate-specific cysteine proteases or caspases. z-VAD.fmk is a cell-permeable fluoromethylketone inhibitor of a broad spectrum of caspases. This in vitro study demonstrates that caspase inhibition can prevent apoptosis in a consistent manner in both bovine and human cartilage. In addition, the associated increase in glycosaminoglycan release seen with loading was also reduced. IGF-1 and dexamethasone also reduced the percentage of cells demonstrating apoptosis. IGF-1 is a major survival factor and is known to protect cells from apoptosis under different conditions. The role of dexamethasone is less clear. Dexamethasone induces apoptosis in certain cells, including T cells, eosinophils, and striatal neurons. However, it has been shown to inhibit apoptosis in lung epithelial cells and neutrophils. One possible mechanism of action that has been postulated is reduction in expression of Fas mRNA. This study demonstrates that both IGF-1 and dexamethasone may play a role in protecting against chondrocyte apoptosis following mechanical injury. These results suggest a potential for a novel pharmacologic modulation of chondrocyte apoptosis and matrix degeneration after mechan­ical injury.
In the present and previous studies1,2, we characterized cartilage response to acute mechanical injury. It appears that chondrocytes undergo apoptosis when subjected to various forms of injury. Both apoptosis and proteoglycan release correlated with load intensity and with each other, suggesting a possible link between apoptosis and matrix loss after mechanical injury. This finding supports the notion that cell death, even in the form of apoptosis, could be linked to matrix loss in cartilage. Since cartilage does not contain tissue macrophages, there is no apparent mechanism for removing dead cells or apoptotic bodies. This raises the possibility that chondrocyte apoptosis could cause further tissue damage and affect subsequent repair. The induction of apoptosis is time-dependent, which offers a therapeutic window during which apoptosis may be inhibited.
The contribution of cell death to cartilage degradation has been previously suggested for human and experimentally induced osteoarthritis, in which a close correlation between the frequency of chondrocyte apoptosis and the severity of osteoarthritic changes was seen. The inhibition of apoptosis as a therapeutic modality may therefore have an even more far-reaching impact on osteoarthritis than the initial preservation of cell viability.
D’Lima DD, Hashimoto S, Chen PC, Lotz MK,Colwell CW Jr. Cartilage injury induces chondrocyte apoptosis. J Bone Joint Surg Am,2001;83(Suppl 2): 19-21. 83(Suppl 2)19  2001 
 
D’Lima DD, Hashimoto S, Chen PC, Lotz MK,Colwell CW Jr. In vitro and in vivo models of cartilage injury. J Bone Joint Surg Am,2001;83(Suppl 2): 22-24. 83(Suppl 2)22  2001 
 

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D’Lima DD, Hashimoto S, Chen PC, Lotz MK,Colwell CW Jr. Cartilage injury induces chondrocyte apoptosis. J Bone Joint Surg Am,2001;83(Suppl 2): 19-21. 83(Suppl 2)19  2001 
 
D’Lima DD, Hashimoto S, Chen PC, Lotz MK,Colwell CW Jr. In vitro and in vivo models of cartilage injury. J Bone Joint Surg Am,2001;83(Suppl 2): 22-24. 83(Suppl 2)22  2001 
 
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These activities have been planned and implemented in accordance with the Essential Areas and policies of the Accreditation Council for Continuing Medical Education (ACCME) through the joint sponsorship of the American Academy of Orthopaedic Surgeons and The Journal of Bone and Joint Surgery, Inc. The American Academy of Orthopaedic Surgeons is accredited by the ACCME to provide continuing medical education for physicians.
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