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DOI: 10.1126/Science.1101074 , 1561 (2004); 306 Science , Et Al. Beth Rise and Fall of the Beringian Steppe Bison Beth Shapiro, et al. Science 306, 1561 (2004); DOI: 10.1126/science.1101074 This copy is for your personal, non-commercial use only. If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here. Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this infomation is current as of April 25, 2011 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/306/5701/1561.full.html Supporting Online Material can be found at: http://www.sciencemag.org/content/suppl/2004/11/22/306.5701.1561.DC1.html on April 25, 2011 A list of selected additional articles on the Science Web sites related to this article can be found at: http://www.sciencemag.org/content/306/5701/1561.full.html#related This article has been cited by 154 article(s) on the ISI Web of Science This article has been cited by 50 articles hosted by HighWire Press; see: http://www.sciencemag.org/content/306/5701/1561.full.html#related-urls This article appears in the following subject collections: www.sciencemag.org Ecology http://www.sciencemag.org/cgi/collection/ecology Downloaded from Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2004 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS. R EPORTS 3). Thus, deletion of JNK2 in macrophages after labeling of JNK2j/j macrophages with 15. A. Daugherty et al., J. Clin. Invest. 100, 1575 (1997). was sufficient to decrease atherogenesis. E32P^ orthophosphoric acid (Fig. 4F). 16. C. Dong et al., Science 282, 2092 (1998). 17. V. J. Dzau, R. C. Braun-Dullaeus, D. G. Sedding, Two receptors appear to be essential in In this study, we provide in vivo evidence Nature Med. 8, 1249 (2002). foam cell formation and receptor-mediated that JNK2 is required in a mouse model of 18. Y. Zhan et al., Arterioscler. Thromb. Vasc. Biol. 23, binding and uptake of modified lipoproteins: atherogenesis. At the molecular level, we 795 (2003). 19. A. C. Li, C. K. Glass, Nature Med. 8, 1235 (2002). CD36 and scavenger receptor A (SR-A) (20). propose that JNK2-dependent decrease of 20. V. V. Kunjathoor et al., J. Biol. Chem. 277, 49982 (2002). Immunofluorescence analyses revealed that SR-A phosphorylation and increase in SR-A 21. S. R. Post et al., J. Lipid Res. 43, 1829 (2002). expression of CD36 was unchanged in abundance may lead to decreased internal- 22. P. J. Gough, D. R. Greaves, S. Gordon, J. Lipid Res. 39, j/j 531 (1998). acLDL-stimulated peritoneal ApoE ization and degradation of receptor-bound 23. P. Tontonoz, L. Nagy, J. G. Alvarez, V. A. Thomazy, JNK2j/j macrophages (Fig. 4A and fig. modified LDL and as a consequence to R. M. Evans, Cell 93, 241 (1998). S7A). However, analyses with antibodies to reduced foam cell formation. Indeed, 24. H. Heider, E. S. Wintergerst, FEBS Lett. 505, 185 (2001). 25. L. G. Fong, D. Le, J. Biol. Chem. 274, 36808 (1999). SR-A showed increased abundance of this macrophage-specific overexpression of SR- 26. N. Kosswig, S. Rice, A. Daugherty, S. R. Post, J. Biol. receptor (Fig. 4B and fig. S7B) (P G 0.01). A has been shown to be sufficient to reduce Chem. 278, 34219 (2003). Protein immunoblotting confirmed increased atherosclerosis in ApoE-deficient mice (27). 27. S. C. Whitman, D. L. Rateri, S. J. Szilvassy, J. A. Cornicelli, A. Daugherty, J. Lipid Res. 43, 1201 (2002). abundance of SR-A in protein extracts In conclusion, specific inhibition of JNK2 28. Macrophages were pulse-labeled with [32P]ortho- prepared from macrophages stimulated with activity may provide a therapeutic approach phosphoric acid in sodium-phosphate-deficient cul- acLDL. Amounts of SR-A were not altered to decrease atheroma formation in patients. ture medium 12 hours before harvesting. 29.WethankP.LerchwhoprovideduswithoxLDL; in response to acLDL in double knockout or D. Zhang and P. Meier, who helped us with iso- j/j j/j control animals (fig. S7C). ApoE JNK2 References and Notes lation of aortas; H. Joch and A. Jaschko, who helped us macrophages formed filopodia-like projec- 1. P. Libby, Nature 420, 868 (2002). with smooth muscle cell isolation; P. Bargsten, who 2. C. K. Glass, J. L. Witztum, Cell 104, 503 (2001). tions, which were not observed in controls helped us with bone marrow transplantation experi- 3. S. Gupta et al., EMBO J. 15, 2760 (1996). ments; W. Krek and P. J. Gough, with whom we had (Fig. 4C). This cellular phenotype is associat- 4. C. Dong et al., Nature 405, 91 (2000). very fruitful scientific discussions; and R. Eferl, for ed with increased adhesion and has been 5. J. Hirosumi et al., Nature 420, 333 (2002). critical reading. Supported by the Swiss National 6. Z. Han, L. Chang, Y. Yamanishi, M. Karin, G. S. Firestein, described in macrophages overexpressing Science Foundation (grant no. 3100-068118), the Arthritis Rheum. 46, 818 (2002). European Union (grant no. G5RD-CT-2001-00532), SR-A (21). To examine whether increased 7. A. M. Manning, R. J. Davis, Nature Rev. Drug Discov. the Bundesamt fu¨r Bildung und Wissenschaft, and the abundance of SR-A in cultured macrophages 2, 554 (2003). Swiss Heart Foundation, and the ‘‘Forschungskredit 8. A. S. Plump et al., Cell 71, 343 (1992). 2003’’ of the University of Zurich. also occurred in vivo, we used immunohisto- 9. Y. S. Heo et al., EMBO J. 23, 2185 (2004). on April 25, 2011 chemistry to detect SR-A on plaques from 10. M. I. Cybulsky et al., J. Clin. Invest. 107, 1255 (2001). Supporting Online Material ApoEj/j JNK2j/j mice and ApoEj/j con- 11. Z. M. Dong, A. A. Brown, D. D. Wagner, Circulation www.sciencemag.org/cgi/content/full/306/5701/1558/ 101, 2290 (2000). DC1 trol mice. Increased amounts of SR-A were de- 12. G. K. Hansson, P. Libby, U. Schonbeck, Z. Q. Yan, Circ. Materials and Methods j/j tected in macrophages in plaques of ApoE Res. 91, 281 (2002). Figs. S1 to S7 JNK2j/j mice compared to those of control 13. D. D. Yang et al., Immunity 9, 575 (1998). References and Notes mice (Fig. 4D). 14. H. M. Dansky, S. A. Charlton, M. M. Harper, J. D. Smith, Proc. Natl. Acad. Sci. U.S.A. 94, 4642 (1997). 23 June 2004; accepted 13 October 2004 Alternative splicing results in three types of SR-A transcripts in humans. Occurrence of the Type III SR-A blocks modified LDL uptake Rise and Fall of the www.sciencemag.org (22). Therefore, we analyzed the expression of all three splicing variants in macrophages by semiquantitative RT-PCR using specific prim- Beringian Steppe Bison ers. We could not detect Type III mRNA in Beth Shapiro,1,2 Alexei J. Drummond,2 Andrew Rambaut,2 macrophages of either genotype. Type I and Michael C. Wilson,3 Paul E. Matheus,4 Andrei V. Sher,5 Type II mRNA was not increased in the ab- 2 1,2 6 sence of JNK2 (fig. S7D). Expression of CD36 Oliver G. Pybus, M. Thomas P. Gilbert, Ian Barnes, 7 1,7 7 or peroxisome proliferator–actived receptor Jonas Binladen, Eske Willerslev, Anders J. Hansen, Downloaded from (PPARg)(23), was also not affected. Activa- Gennady F. Baryshnikov,8 James A. Burns,9 Sergei Davydov,10 tion of the well-known JNK target c-jun in Jonathan C. Driver,11 Duane G. Froese,12 C. Richard Harington,13 j j j j j j aortas from ApoE / and ApoE / JNK2 / Grant Keddie,14 Pavel Kosintsev,15 Michael L. Kunz,16 mice fed either a normal or high-cholesterol Larry D. Martin,17 Robert O. Stephenson,18 John Storer,19 diet was not affected, suggesting that c-jun- 20 10 1,2* dependent gene expression was not impaired Richard Tedford, Sergei Zimov, Alan Cooper (fig. S7E). Phosphorylation of SR-A on spe- The widespread extinctions of large mammals at the end of the Pleistocene cific serines is essential for SR-A–dependent epoch have often been attributed to the depredations of humans; here we processing of modified LDL and for surface present genetic evidence that questions this assumption. We used ancient DNA expression of SR-A (24–26). We immunopre- and Bayesian techniques to reconstruct a detailed genetic history of bison cipitated SR-A from total protein extracts of throughout the late Pleistocene and Holocene epochs. Our analyses depict a JNK2j/j macrophages and corresponding wild- large diverse population living throughout Beringia until around 37,000 years type cells. Western blotting of immunopre- before the present, when the population’s genetic diversity began to decline cipitated SR-A revealed an increased amount dramatically. The timing of this decline correlates with environmental changes of SR-A in JNK2j/j cells compared to wild- associated with the onset of the last glacial cycle, whereas archaeological type cells (Fig. 4, E and F). Blotting with evidence does not support the presence of large populations of humans in phosphoserine-specific antibody indicated that Eastern Beringia until more than 15,000 years later. the amount of serine-phosphorylated SR-A was lower in JNK2j/j extracts even though Climatic and environmental changes during (ky B.P.)^ played an important role in the more SR-A protein was present (Fig.
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