Class Note for SOC 101 at UA
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398 REPORTS precursors containing simple alkyl esters un derwent Michael addition but the resulting adducts did not cyclize Perhaps even more re markable than the condensation that produces 21 is the parallel transformation of 20 with the enone 4 Fig 3 entry 1 which forms 6 deoxytetracycline 6 in protected form with gt201 diastereoselectivity in 81 yield a er puri cation by RP HPLC diastereomer ically pure a minor diastereomer epimeric at C6 was also isolated separately It appears that additions to 4 and 5 proceed almost exclusively by addition to one face of each enone the top face as drawn in Fig 1B producing CSa stereochemistry corresponding to that of natural tetracyclines although why this should be the case is not obvious Ef cient and stereoselective condensations were not restricted to the 0 toluate anion derived from the Dring substrate 20 In all we prepared six 6 deoxytetracycline variants Fig 3 In each case it was necessary to op timize the specific conditions for 0 toluate anion generation and trapping For the synthe sis of products 8 9 and 10 Fig 3 anion generation was best conducted in situ in the presence of the enone 4 either by selective deprotonation 8 or by lithium halogen ex change 9 and 10 A number of potentially competing nonproductive reaction sequences might have intervened during in situ anion generation such as enolization of 4 the ob served efficiencies ofthe transformations are surprising in light of this It is also note worthy that in situ anion generation permits the use of 0 toluates lacking an 0 alkoxy substituent such as used in the synthesis of 8 and 9 substrates that are known to be problematic from prior studies 35 Also lithium halogen exchange reactions of ben zylic halides such as used in the synthesis of 9 and 10 had previously been considered impracticable 36 37 The e iciencies of the synthetic sequences we report have allowed for the preparation of sufficient quantities of each tetracycline analog for antibacterial testing using stan dard serial dilution techniques in 5 to 20 mg amounts Minimum inhibitory concentrations MICs were determined for each analog in whole cell antimicrobial assays using five Gram positive and ve Gram negative or ganisms Fig 3 Thus far the pentacycline derivative 10 has shown the most promising antibacterial properties with activity equal to or greater than tetracycline in each of the Gram positive strains examined including strains with resistance to tetracycline methicillin and vancomycin Although this finding is note worthy it is very likely that antibiotics with even greater potencies andor improved pharmacological properties will emerge with further exploration of the complex chemical space now made accessible by the versatile synthetic route described References and Notes 1 C Walsh Antibiotics Actions Origins Resistance American Society for Microbiology Press Washing ton DC 2003 2 s c B Amyes Magic Bullets Lost Horizons the Rise and Fall ofAntibibtics Taylor and Francis New York 2001 3 M Leeb Nature 431 892 2004 4 w R Strohl Metab Eng 3 4 2001 5 D E Cane C T Walsh C Khosla Science 282 63 1998 6 L Katz Chem Rev 97 2557 1997 7 c R Stephens et a j Am Chem Soc 85 2643 1963 8 M Nelson W Hillen R A Greenwald Eds Tetracyclines in Biology chemistry and Medicine Birkhauser Verlag Boston 2001 9 D E Brodersen et a Cell 103 1143 2000 10 M Pioletti et a EMBO j 20 1829 2001 11 PE Sum P Petersen Bioorg Med Chem Lett 9 1459 1999 12 K Bush M Macielag M WeidnerWells Curr Opin Microbiol 7 455 2004 13 i Korst etal Am Chem Soc 90 439 1968 14 A l Gurevich et a Tetrahedron Lett 8 131 1967 15 H Muxfeldt et aj Am Chem Soc 101 689 1979 16 K Talsuta T Voshimoto H Gunji V Okado M Takahashi Chem Lett jpn 2000 545 2000 17 c Stork La Clair P Spargo R P Nargund N Totah j Am Chem Soc 118 5304 1996 18 w Rogalski in Handbook of Experimental Pharma cology Hlavka H Boothe Eds Springer Verlag New York 1985 vol 78 chap 5 19 A M Reiner G D Hegeman Biochemistry 10 2530 1971 20 A G Myers D R Siegel D J Buzard M G Charest Org Lett 3 2923 2001 21 G Stork A A Hagedorn H j Am Chem Soc 100 3509 1978 22 D M Vyas v chiang T w Doyle Tetrahedron Lett 25 487 1984 23 P Pevarello M Varasi Synth Commun 22 1939 1992 24 s H Pine Org React 18 403 1970 25 A G Myers B Zheng Tetrahedron Lett 37 4841 1996 25 M Frigerio M Santagostino Tetrahedron Lett 35 8019 1994 27 E Corey H cho c Rucker D H Hua Tetrahedron Lett 22 3455 1981 28 F A Davis M c Weismiller c K Murphy R T Reddy Bc Chen j Org Chem 57 7274 1992 29 E N Prilezhaeva Russ Chem Rev 70 897 2001 30 TL Ho Tandem Organic Reactions Wiley New York 1992 31 F Leeper Staunton j Chem Soc Chem Comm 1978 405 1978 32 F M Hauser R P Rhee j Org Chem 43 178 1978 33 i H Dodd 5 M Weinreb Tetrahedron Lett 20 3593 1979 34 i D white E c Nolen r c H Miller Org Chem 51 1150 1986 35 F M Hauser R P Rhee s Prasanna s M Weinreb H Dcdd Synthesis Mass 1980 72 1980 35 w E Parham L D Jones v A Sayed j Org Chem 41 1184 1976 37 s c Berk M c P Veh N eong P Knochel Organornetaiiics 9 3053 1990 38 We thank D Kahne and c Wa 1 for helpful discussions and w Brubaker Farmington Pharma Development and c Thoma and Thanass39 Achillion Pharmacue ticais for antibacterial screening This work was supported by NiH grant Al48825 NSF predoctoral graduate fellowships MGC and DB and the Deutscher Akademischer Austausch Dienst CDL AGM serves on the scientiiic advisory boards of Vicuron Pharmaceuticals and Miikana Therapeutics and is a consultant for Pfizer The research described here is independent Supporting Online Material wwwsciencemagorgcgicontentfull3085720395 DC l Materials and Methods References 13 January 2005 accepted 1 March 2005 101126science1109755 Hypoxia Global Warming and Terrestrial Late Permian Extinctions Raymond B Hueyquot and Peter D Ward A catastrophic extinction occurred at the end of the Permian Period However baseline extinction rates appear to have been elevated even before the final catastrophe suggesting sustained environmental degradation For terrestrial vertebrates during the Late Pennian the combination of a drop in atmospheric oxygen plus climate warming would have induced hypoxic stress and consequently compressed altitudinal ranges to near sea level Our simulations suggest that the magnitude of altitudinal compression would have forced extinctions by reducing habitat diversity fragmenting and isolating populations and inducing a speciesarea effect It also might have delayed ecosystem recovew after the mass extinction A catastrophic extinction marks the end of the Permian 1 2 and is attributed to an acute climate crisis among other causes 3 5 However background extinction rates and ecosystem turnover were elevated throughout much of the Late Permian 6 7 and recovery a er extinction was slow 1 2 Thus en vironmental degradation likely occurred both before and after the final catastrophe perhaps caused by major shi s in atmospheric chem istry 8 Indeed modeling isotope and paleontological evidence 9 13 suggests that 02 levels plummeted in the Late Permian and Early Triassic Fig 1A and would have restricted the supply of 02 to organisms At the same time CO2 levels were rising Fig 1A and climate warming 14 would have increased metabolic demand for 02 Severe hypoxia was inevitable 9 15 16 Here we explore a biogeographic conse quence of presumed low 02 levels during the Late Permian and Triassic Terrestrial animals 15APRL 2005 VOL308 SCIENCE wwwsciencemagorg would have been restricted to low altitude because even moderate altitudes would have insuf cient 02 We simulate the magnitude of altitudinal compression and evaluate its con tributions to the high background extinction rate the catastrophic extinction and the delayed recovery 1 2 Terrestrial animals attempting to live at moderate to high altitude are physiologically challenged by declining temperatures food supply habitat area and 02 levels along with increased respiratory water loss 1 7 The upper altitudinal limits of species likely re ect the in uence of these factors as well as ecological geological and biogeographic factors 18 The relative contribution of O2 in limiting altitudinal ranges has no doubt changed over time because 02 levels uctuated so drastical ly Fig 1A For example when 02 levels appear to have been at their zenith during the cold Early Permian 3OO million years ago lVIa Fig 1A the partial pressure of inspired 02 P102 even at an altitude of 6 km may have matched that at sea level in today s atmosphere 19 In this glaciated and 02 rich environment altitudinal ranges would have been constrained by extreme cold or ice not by 02 levels But when 02 levels are calculated to be at their nadir during the hot Early Triassic 240 and 200 Ma PIO2 even at sea level may have been equivalent to that at 253 km in today s atmosphere Fig 1B If estimates of 02 Fig 1A and climate are correct the combination of low PIO2 and high temperature would have induced hypoxia and restricted terrestrial vertebrates to low altitudes We simulated the impact of 02 levels on maximum altitudinal ranges of vertebrates having a presumed mid Permian physiology 20 The actual hypoxia tolerance of mid Permian ectotherms is of course unknown but was probably lower than that of present day vertebrates Mid Permian vertebrates not only had primitive respiratory systems 9 but also had been evolving in an 02 rich atmosphere for millions of years Fig 1A and could not have become adapted to altitude hence to low 02 levels because of icehouse temper atures during that time We start by deriving a reference set of hypothetical species living in the mid Permian and having maximum altitudes ranging from 20 to 80 km in 1 km intervals We assume that the maximum altitude of each species was set by or at least strongly in uenced by the critical PIO2 occurring at that altitude Then assuming that hypoxia tolerances were con stant over time ie always had the same critical P102 we calculate how maximum Department of Biology University of Washington Box 351800 Seattle WA 98195 USA To whom correspondence should be addressed E mail hueyrbuwashingtonedu wwwsciencemagorg SCIENCE VOL308 altitudes Fig 1C changed with 02 levels Fig 1A This involves estimating the aver age PIO2 at each altitude during the mid Permian and then computing at intervals of 10 million years the altitude where each PIO2 would have occurred 20 The presumed drop in 02 levels during the Late Permian Fig 1A would have drastically compressed the altitudinal ranges of all hypothetical species Fig 1C If 02 levels dropped to 16 at the end of the Permian 8 PIO2 at sea level would have been equivalent to that found today at 27 km Animals with limited hypoxia tolerance would have gone extinct Fig 1C To survive a species would have needed to tolerate a PIO2 at least equivalent to that found at 60 km red line Fig 1C in the mid Permian 2 22 02 levels are thought to have continued to drop into the Early Triassic and to have stayed relatively low for the next 100 million years REPORTS Fig 1A In addition CO2 levels Fig 1A and global temperatures 14 remained high Thus hypoxia and the resultant altitudinal compression likely persisted into the early Cretaceous Fig 1 A and C and may have contributed to a slow recovery after the mass extinction 1 2 Our simulations Fig 1 B and C focus on 02 levels but rising temperatures in the Late Permian and Early Triassic 14 would have exacerbated hypoxia To reduce the impact ectotherms could have dispersed along sea level corridors to high latitudes thereby lowering their body temperatures Alternative ly they could have invaded relatively cool aquatic habitats Indeed air breathing aquatic reptiles eg ichthyosaurs phytosaurs di versified at this time Freshwater breathing ectotherms were al so probably restricted to low altitudes during 02 lows Reduced atmospheric 02 levels 30 25 s 1 Percentage 02 amp R C02 F3AL R00 6 a IfOISIID ij TrIIJI KII Fig 1 A Percent 02 over time green and the concentration of CO2 gray relative to present day level PAL of each gas is indicated Global hypoxia would have occurred in the Late Permian and Triassic because of dropping 02 combined with rising temper atures data from 4 The mass extinction at the Permian Triassic boundary is indicated by quotquots a red dashed line B Present day T quotJ altitude with PO2 equivalent to 500 400 300 200 Time Ma 100 0 that at sea level in the Phanero zoic Thus PO2 at sea level at the Triassic 02 minimum would be found today at 5 kmr C sea level 0 TI39IJI K Predicted maximum altitude over time for hypothetical species having graded tolerances 2 to 8 km to hypoxia From the Late Permian through the Jurassic however PO2 was sufficiently low that ranges would have been compressed to near sea level and some species would have gone extinct Period codes 6 Cambrian O Ordovician S Silu rian D Devonian C Carbonifer ous P Permian Tr Triassic J Current altitude equivalent km 6 os D c I 500 400 300 200 Time Ma i I 100 0 Jurassic K Cretaceous T Tertiary sea level 2km Maximum altitude km 250 Time Ma 15 APRIL 2005 399 400 REPORTS plus warm water temperatures would lower aquatic 02 levels but warm body temper atures increase 02 demand Thus water breathing ectotherms would likely have been 02 challenged even near sea level Insects which su ered major extinctions during the Late Permian 23 might also have experienced some hypoxia and altitudinal compression Insect development is slowed by low PO2 plus warm temperatures 24 Inter estingly giant dragon ies which evolved during the Permian 02 high are thought to have gone extinct in the Late Permian because of limitations on O2 diffusion 9 However today s large adult insects rely on convec tive ventilation and are remarkably hypoxia tolerant 25 thus the aquatic larvae of giant insects may have been the primary targets of hypoxia induced extinction Altitudinal compression would have had important biogeographic consequences Ani mals specialized for upland habitats could not have survived as they would have been physiologically excluded from them More over mountain passes would have seemed physiologically higher to animals 26 than are passes of equivalent altitude today Thus populations would have become fragmented and isolated fig S2 and rates of local extinction may have increased 2 7 Altitudinal compression plus rising sea levels at the very end of the Permian I4 28 would have also reduced the land surface physiologically accessible to animals This loss would have caused additional extinctions via a species area effect 29 and also would have delayed the recovery Topographic maps for the mid Permian to Late Permian 30 enable us to estimate 20 albeit with substantial uncertainty the per centage of the land surface that was physio logically accessible to animals with specified hypoxia tolerance Fig 2 During the 02 high in the Permian virtually the entire surface of Earth had sufficient O2 to sustain populations of our hypothetical species By the Triassic however hypoxia would have reduced acces Fig 2 Plot of cumulative land area 100 versus physical altitude during the mid Permian to Late Permian solid line 30 and for the present day dashed line 20 This relationship enables us to estimate the per centage of the land surface that was physiologically tolerable 20 for the hypothetical species shown in Fig 1C A species capable of surviving up to 60 km in the mid Permian would been restricted to below 03 km by the end of the Permian gray dotted line and thus would have been able to 07 80 D O 1 Cumulative area 4 P 20 sible land area for all but the most hypoxia tolerant species Fig 1C For example a species physiologically capable of surviving up to 60 km in the mid Permian would have been restricted to below 03 km by the Triassic thus it would have been excluded from more than half of the available land surface gray dotted line in Fig 2 By the early Triassic Fig 1A even a species that could tolerate 80 km in the mid Permian would have likely gone extinct Fig 1C in the absence of compensatory adaptation Thus altitudinal compression could have had sub stantial effects on extinction and recovery rates given the huge loss in land for all but the most hypoxia resistant taxa Fig 2 The reasonableness of our scenario of hypoxia induced altitudinal compression de pends fundamentally on the accuracy and timing of estimates of percent 02 8 Those estimates of course have uncertainty 8 20 and other models can yield somewhat differ ent estimates 2 3 Our analyses also assume that 02 restricted the upper altitudinal limits during the Late Permian and Triassic that terrestrial verte brates then had modest hypoxia tolerance and that adaptation to hypoxia was limited None of these assumptions can be directly tested as yet but our compression hypothesis leads to predictions and patterns that are subject to test 1 Terrestrial vertebrates that did survive the Late Permian should show respiratory adaptations for hypoxia Indeed morphologi cal traits of Lystrosaums one of the few surviving therapsids and of other Triassic dicynodonts have been interpreted as adapta tions to hypoxia 6 3l 2 Hyperventilation in response to hypoxia would have elevated respiratory water loss during the Late Permian Maxilloturbinates which reduce respiratory water loss first evolved at that time in mammal like reptiles 32 Turbinates have been interpreted as in dicating high respiratory rates associated with endothermy 32 but they might also be midlate Permian quot present day occupy less than half of the 0 available land area Less hypoxia tolerant species would have gone 10 20 30 Physical altitude km extinct more tolerant ones would have suffered minimal area loss indicators of high respiratory rates induced by hypoxia 3 Fossil sites for terrestrial ectotherms by the Triassic should be located predominantly at high latitude where relatively cooler temperatures would reduce metabolic require ments for O2 and ameliorate hypoxia Distri butional data for therapsids are consistent 33 However therapsids might also have been restricted to high latitude simply because low latitude sites were hot dry and had a depauperate ora 34 4 The compression forced isolation of taxa into refugia could help to explain Late Permian endemism 33 which is surprising for a Pangaean supercontinent It could also help to explain the Lazarus effect ie the reappearance of taxa that disappeared from the fossil record noted in this period I 35 The extinctions during the Late Permian were the largest ever during the history of life on Earth An abrupt climate change is thought to be responsible for the catastrophic extinc tion Nonetheless hypoxia may have contrib uted to the high background extinctions and high faunal turnover occurring before the mass extinction to the final catastrophe itself and to the delayed recovery Low 02 levels would have promoted extinction and delayed recovery directly via physiological stress 16 and indirectly via altitudinal compression Note added in proof A forthcoming paper 36 provides new and fine scaled estimates of 02 levels during the Late Permian and Early Triassic The drop in 02 during the Late Permian is slightly more recent than that in Fig 1A but still suggests that hypoxia and altitudinal compression were influential both before and after the mass extinction References and Notes 1 D H Erwin The Great Paleozoic Crisis Columbia Univ Press New York 1993 2 S A Bowring D H Erwin Y lsozaki Proc Natl Acad Sci USA 96 8827 1999 3 A H Knoll R K Bambach D E Canfield J P Grotzinger Science 273 452 1996 4 R A Berner Proc Natl Acad Sci USA 99 4172 2002 5 M J Benton R J Twichett Trends Ecol Evol 18 358 2003 6 M J Benton V P Tverdokhlebov M V Surkov Nature 432 97 2004 7 P D Ward et al Science 307 709 2005 published online 20 January 2005 101126science1107068 8 R A Berner Geochim Cosmochim Acta 65685 2001 9 J B Graham R Dudley N Aguilar C Gans Nature 375 117 1995 10 A C Lasaga H Ohmoto Geochim Cosmochim Acta 66 361 2002 11 N D Sheldon G J Retallack Geology 30 919 2002 12 N M Bergman T M Lenton A J WatsonAm 1 Sci 304 397 2004 13 R A Berner The Phanerozoic Carbon Cycle C02 and 02 Oxford Univ Press Oxford 2004 14 D L Kidder T R Worsley Palaeogeogr Palaeoclimatol Palaeoecol 203 207 2004 15 R A Berner D J Beerling R Dudley J M Robinson R A Wildman Jr Annu Rev Earth Planet Sci 31 105 2003 16 G J Retallack R M H Smith P D Ward Geol Soc Am Bull 115 1133 2003 15 APRIL 2005 VOL 308 SCIENCE www5ciencemagorg 17 P Bouverot Adaptation to Altitude Hypoxia in Vertebrates SpringerVerlag Berlin 1985 13 K Gaston The Structure and Dynamics of Geographic Ranges Oxford Univ Press Oxford 2003 19 We estimate PioZ rather than P02 because the addition of respiratory water vapor reduces the partial pressure of 02 in the lung 20 20 See supporting data on Science Online 21 Estimates of maximum altitudes for the Late Permian and Triassic are somewhat low because warm temperatures would have elevated barometric pres sure at altitude However the impact on 02 would have been small Substituting P02 and temperature estimates in the hypsometric equation demonstrates that our altitudinal estimates for the Triassic 02 low Fig 1c underestimate actual limits by at most 01 km 22 Similarly our estimates of maximum altitudes in the cold midPermian Fig 1c overestimate actual limits by at most 02 km 22 Because these effects are relatively small we ignore them in our simulations 22 D Battisti personal communication 23 c c Labandeira Sepkoski r Science 251 310 1993 24 M R Frazier H A Woods F Harrison Physiol Biochem Zool 74 541 2001 25 K Greenlee F Harrison j Exp Biol 207 497 2004 25 D H lanzenArn Nat 101 233 1957 27 l A Hanski Metapopulation Ecology Oxford Univ Press Oxford 1999 28 A Hallam P B Wignall Earth Sci Rev 43 217 1999 29 M L Rosenzweig Species Diversity in Space and Time Cambridge Univ Press Cambridge 1995 30 D B Rowley R T Pierrehumbert B S Currie Earth Planet Sci Lett BB 253 2001 31 K Angielczyk personal communication 32 W Hillenius A Ruben Physiol Biochem Zool 77 1019 2004 33 c A Sidor et al Nature in press 34 P M Rees Geology 30 827 2002 35 P B Wignall M Benton j Geol Soc London 155 453 1999 35 R A Berner Ceachim Cosmochim Acta in press OpenSystem Coral Ages Reveal Persistent Suborbital SeaLevel Cycles William C Thompsonquot and Steven L Goldstein Sea level is a sensitive index of global climate that has been linked to Earth s orbital variations with a minimum periodicity of about 21000 years Although there is ample evidence for climate oscillations that are too frequent to be explained by orbital forcing suborbitalfrequency sealevel change has been difficult to resolve primarily because of problems with uraniumthorium coral dating Here we use a new approadi that corrects coral ages for the frequently observed opensystem behavior of uraniumseries nuclides substantially improving the resolution of sealevel reconstruction This curve reveals persistent sealevel oscillations that are too frequent to be explained ex clusively by orbital forcing The idea that Quaternary climate cycles are linked to changes in Earth s orbit is central to climate change theory 1 The primary evi dence for this comes from the marine oxygen isotope 5130 record 2 and early dating of coral terraces 3 However there is abun dant evidence for abrupt climate change that was too frequent to be explained by orbital changes 4 Here we attempt to reconstruct sea level between 70 and 240 thousand years ago ka with a resolution sufficient to detect suborbital frequency oscillations using a new approach to UTh coral dating 5 Sev eral recent lines of evidence suggest that sea level may be more variable than previously thought An example is the conversion via a hydraulic model of a salinity record from the Red Sea into a sea level curve for the past 470 Lamont Doherty Earth Observatoly LDEO and Department of Earth and Environmental Sciences Columbia University Palisades NY 10964 USA Present address Department of Geology and Geo physics 118 Clark Lab Mail Stop 23 Woods Hole Oceanographic Institution Woods Hole MA 02543 USA TTo whom correspondence should be addressed E mail wthompsonwhoiedu www5ciencemagorg SCIENCE VOL308 thousand years ky 6 This record suggests fairly large 35 m suborbital frequency sea level changes during glacial periods such as marine isotope stage 3 MIS 3 and more mod est 15 m changes during interglacials for example during MIS 5 This new Red Sea record augments a growing body of evidence for suborbital sea level uctuations in coral records At the Huon Peninsula of Papua New Guinea multiple coral terraces were formed during MIS 3 with highstands occurring about every 6 ky 7 8 There are also more Huon terraces associated with MIS 5 than can be accounted for by orbital variability 9 Such evidence is not restricted to New Guinea closely spaced terraces on Barbados suggest suborbital period changes in sea level during MIS 5a and MIS 5c 9 10 The construction of a high resolution sea level record requires a large number of ac curate coral ages from a limited geographic area and this has not been possible with standard dating methods The conventional equations for UTh age determination 1 require that loss or gain of U and Th have not occurred except by radioactive decay a er coral death This closed system requirement 15 APRIL 2005 REPORTS 37 R A Berner z KothavalaArn j Sci 301 182 2001 38 We thank R Berner for providing data advice and discussion K Angielczyk M Benton R Buick c Carey T Daniel R Dudley D Erwin Graham T Hornbein D Rowley Ruben A Smith M Stoeck and West for discussion D Battisti for computing the impact of temperature on critical altitudes and D Rowley and 0 Wang for calculating hypsometric data Supported by NSF grant IBN0416843 RBH and the NASA Astrobiology institute University of Washington Node PDW principal investigator Supporting Online Material www5ciencemagorgcgicontentfull3085720398 DC I Materials and Methods Figs S1 and 52 References 29 November 2004 accepted 15 February 2005 IO I126science l108019 is often violated in fossil corals as a result of the alpha recoil mobility of U series nuclides 12 and an initial coral 234U23 3U ratio that is significantly different from that of modern seawater is taken as evidence of open system behavior and an unreliable age 13 Building on earlier attempts to correct for open system behavior 14 we have derived a set of decay equations that corrects coral ages for these effects 5 Although conventional U series coral ages from a single stratigraphic level o en differ substantially open syst
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