Elephantid Genomes Reveal the Molecular Bases of Woolly Mammoth Adaptations to the Arctic

Cell Reports

Volumn 12, Issue 2, 2015, Pages 217-228

  Lynch, Vincent J ^a   Bedoya Reina, Oscar C ^b,c   Ratan, Aakrosh ^b,d   Sulak, Michael ^a   Drautz Moses, Daniela I ^b,e   Perry, George H ^b   Miller, Webb ^b   Schuster, Stephan C ^b,e  

^a UNIVERSITY OF CHICAGO   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF VIRGINIA   (United States)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

VANILLOID RECEPTOR 3; VANILLOID RECEPTOR;

ADIPOGENESIS; AMINO ACID SUBSTITUTION; ARCTIC; ARTICLE; CIRCADIAN RHYTHM; COLD ACCLIMATIZATION; CONTROLLED STUDY; EAR; ELEPHANT; EVOLUTIONARY ADAPTATION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENOME ANALYSIS; HAIR GROWTH; LIPID METABOLISM; MAMMOTH; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; SKIN; SKIN FUNCTION; TEMPERATURE SENSITIVITY; TRPV3 GENE; ADAPTATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; GENETICS; GENOME; HEK293 CELL LINE; HIGH THROUGHPUT SEQUENCING; HUMAN; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PROTEIN TERTIARY STRUCTURE;

ELEPHANTIDAE; ELEPHAS MAXIMUS; MAMMUTHUS PRIMIGENIUS;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ARCTIC REGIONS; ELEPHANTS; EVOLUTION, MOLECULAR; GENOME; HEK293 CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MAMMOTHS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; TRPV CATION CHANNELS;

EID: 84937519443     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.027     Document Type: Article

References (84)

1. Adzhubei I.A., Schmidt S., Peshkin L., Ramensky V.E., Gerasimova A., Bork P., Kondrashov A.S., Sunyaev S.R. A method and server for predicting damaging missense mutations. Nat. Methods 2010, 7:248-249.
2. Adzhubei I., Jordan D.M., Sunyaev S.R. Predicting functional effect of human missense mutations using PolyPhen-2. Curr. Protoc. Hum. Genet. 2013, Chapter 7:7.20.
3. Aneiros E., Dabrowski M. Novel temperature activation cell-based assay on thermo-TRP ion channels. J. Biomol. Screen. 2009, 14:662-667.
4. Aubdool A.A., Graepel R., Kodji X., Alawi K.M., Bodkin J.V., Srivastava S., Gentry C., Heads R., Grant A.D., Fernandes E.S., et al. TRPA1 is essential for the vascular response to environmental cold exposure. Nat. Commun. 2014, 5:5732.
5. Bautista D.M., Siemens J., Glazer J.M., Tsuruda P.R., Basbaum A.I., Stucky C.L., Jordt S.-E., Julius D. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 2007, 448:204-208.
6. Bedoya-Reina O.C., Ratan A., Burhans R., Kim H.L., Giardine B., Riemer C., Li Q., Olson T.L., Loughran T.P., Vonholdt B.M., et al. Galaxy tools to study genome diversity. Gigascience 2013, 2:17.
7. Blake J.A., Bult C.J., Eppig J.T., Kadin J.A., Richardson J.E. The Mouse Genome Database: integration of and access to knowledge about the laboratory mouse. Nucleic Acids Res. 2014, 42:D810-D817. Mouse Genome Database Group.
8. Bloch G., Barnes B.M., Gerkema M.P., Helm B. Animal activity around the clock with no overt circadian rhythms: patterns, mechanisms and adaptive value. Proc. Biol. Sci. 2013, 280:20130019.
9. Boeskorov G.G., Tikhonov A.N., Lazarev P.A. A new find of a mammoth calf. Dokl. Biol. Sci. 2007, 417:480-483.
10. Borbíró I., Lisztes E., Tóth B.I., Czifra G., Oláh A., Szöllosi A.G., Szentandrássy N., Nánási P.P., Péter Z., Paus R., et al. Activation of transient receptor potential vanilloid-3 inhibits human hair growth. J. Invest. Dermatol. 2011, 131:1605-1614.
11. Campbell K.L., Roberts J.E.E., Watson L.N., Stetefeld J., Sloan A.M., Signore A.V., Howatt J.W., Tame J.R.H., Rohland N., Shen T.-J., et al. Substitutions in woolly mammoth hemoglobin confer biochemical properties adaptive for cold tolerance. Nat. Genet. 2010, 42:536-540.
12. Cao E., Liao M., Cheng Y., Julius D. TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 2013, 504:113-118.
13. Chan Y.F., Marks M.E., Jones F.C., Villarreal G., Shapiro M.D., Brady S.D., Southwick A.M., Absher D.M., Grimwood J., Schmutz J., et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 2010, 327:302-305.
14. Chappuis S., Ripperger J.A., Schnell A., Rando G., Jud C., Wahli W., Albrecht U. Role of the circadian clock gene Per2 in adaptation to cold temperature. Mol. Metab. 2013, 2:184-193.
15. Chen J., Kang D., Xu J., Lake M., Hogan J.O., Sun C., Walter K., Yao B., Kim D. Species differences and molecular determinant of TRPA1 cold sensitivity. Nat. Commun. 2013, 4:2501.
16. Cheng X., Jin J., Hu L., Shen D., Dong X.P., Samie M.A., Knoff J., Eisinger B., Liu M.L., Huang S.M., et al. TRP channel regulates EGFR signaling in hair morphogenesis and skin barrier formation. Cell 2010, 141:331-343.
17. Cheung S.Y., Huang Y., Kwan H.Y., Chung H.Y., Yao X. Activation of transient receptor potential vanilloid 3 channel suppresses adipogenesis. Endocrinology 2015, 156:2074-2086.
18. Chung M.-K., Lee H., Mizuno A., Suzuki M., Caterina M.J. TRPV3 and TRPV4 mediate warmth-evoked currents in primary mouse keratinocytes. J. Biol. Chem. 2004, 279:21569-21575.
19. Cooper G.M., Shendure J. Needles in stacks of needles: finding disease-causal variants in a wealth of genomic data. Nat. Rev. Genet. 2011, 12:628-640.
20. Debruyne R., Chu G., King C.E., Bos K., Kuch M., Schwarz C., Szpak P., Gröcke D.R., Matheus P., Zazula G., et al. Out of America: ancient DNA evidence for a new world origin of late quaternary woolly mammoths. Curr. Biol. 2008, 18:1320-1326.
21. del Camino D., Murphy S., Heiry M., Barrett L.B., Earley T.J., Cook C.A., Petrus M.J., Zhao M., D'Amours M., Deering N., et al. TRPA1 contributes to cold hypersensitivity. J. Neurosci. 2010, 30:15165-15174.
22. Delport W., Poon A.F., Frost S.D., Kosakovsky Pond S.L. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26:2455-2457.
23. DePristo M.A., Banks E., Poplin R., Garimella K.V., Maguire J.R., Hartl C., Philippakis A.A., del Angel G., Rivas M.A., Hanna M., et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 2011, 43:491-498.
24. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
25. Fisher D.C., Tikhonov A.N., Kosintsev P.A., Rountrey A.N., Buigues B., van der Plicht J. Anatomy, death, and preservation of a woolly mammoth (Mammuthus primigenius) calf, Yamal Peninsula, northwest Siberia. Quat. Int. 2012, 255:94-105.
26. Flicek P., Ahmed I., Amode M.R., Barrell D., Beal K., Brent S., Carvalho-Silva D., Clapham P., Coates G., Fairley S., et al. Ensembl 2013. Nucleic Acids Res. 2013, 41:D48-D55.
27. Gilbert M.T.P., Tomsho L.P., Rendulic S., Packard M., Drautz D.I., Sher A., Tikhonov A., Dalén L., Kuznetsova T., Kosintsev P., et al. Whole-genome shotgun sequencing of mitochondria from ancient hair shafts. Science 2007, 317:1927-1930.
28. Gilbert M.T.P., Drautz D.I., Lesk A.M., Ho S.Y.W., Qi J., Ratan A., Hsu C.-H., Sher A., Dalén L., Götherström A., et al. Intraspecific phylogenetic analysis of Siberian woolly mammoths using complete mitochondrial genomes. Proc. Natl. Acad. Sci. USA 2008, 105:8327-8332.
29. Goecks J., Nekrutenko A., Taylor J. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 2010, 11:R86. Galaxy Team.
30. Grandl J., Hu H., Bandell M., Bursulaya B., Schmidt M., Petrus M., Patapoutian A. Pore region of TRPV3 ion channel is specifically required for heat activation. Nat. Neurosci. 2008, 11:1007-1013.
31. Henikoff S., Henikoff J.G. Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. USA 1992, 89:10915-10919.
32. Hoekstra H.E., Hirschmann R.J., Bundey R.A., Insel P.A., Crossland J.P. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 2006, 313:101-104.
33. Huang S.M., Li X., Yu Y., Wang J., Caterina M.J. TRPV3 and TRPV4 ion channels are not major contributors to mouse heat sensation. Mol. Pain 2011, 7:37.
34. Imura K., Yoshioka T., Hikita I., Tsukahara K., Hirasawa T., Higashino K., Gahara Y., Arimura A., Sakata T. Influence of TRPV3 mutation on hair growth cycle in mice. Biochem. Biophys. Res. Commun. 2007, 363:479-483.
35. Inoue I., Yanai K., Kitamura D., Taniuchi I., Kobayashi T., Niimura K., Watanabe T., Watanabe T. Impaired locomotor activity and exploratory behavior in mice lacking histamine H1 receptors. Proc. Natl. Acad. Sci. USA 1996, 93:13316-13320.
36. Kanehisa M., Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000, 28:27-30.
37. Karashima Y., Talavera K., Everaerts W., Janssens A., Kwan K.Y., Vennekens R., Nilius B., Voets T. TRPA1 acts as a cold sensor in vitro and in vivo. Proc. Natl. Acad. Sci. USA 2009, 106:1273-1278.
38. Kim A.Y., Tang Z., Liu Q., Patel K.N., Maag D., Geng Y., Dong X. Pirt, a phosphoinositide-binding protein, functions as a regulatory subunit of TRPV1. Cell 2008, 133:475-485.
39. Kim S.E., Patapoutian A., Grandl J. Single residues in the outer pore of TRPV1 and TRPV3 have temperature-dependent conformations. PLoS One 2013, 8:e59593.
40. Kircher M., Sawyer S., Meyer M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 2012, 40:e3.
41. Knowlton W.M., Bifolck-Fisher A., Bautista D.M., McKemy D.D. TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo. Pain 2010, 150:340-350.
42. Krause J., Dear P.H., Pollack J.L., Slatkin M., Spriggs H., Barnes I., Lister A.M., Ebersberger I., Pääbo S., Hofreiter M. Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae. Nature 2006, 439:724-727.
43. Kwan K.Y., Allchorne A.J., Vollrath M.A., Christensen A.P., Zhang D.-S., Woolf C.J., Corey D.P. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 2006, 50:277-289.
44. Lalueza-Fox C., Römpler H., Caramelli D., Stäubert C., Catalano G., Hughes D., Rohland N., Pilli E., Longo L., Condemi S., et al. A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals. Science 2007, 318:1453-1455.
45. Lang M., Murat S., Clark A.G., Gouppil G., Blais C., Matzkin L.M., Guittard E., Yoshiyama-Yanagawa T., Kataoka H., Niwa R., et al. Mutations in the neverland gene turned Drosophila pachea into an obligate specialist species. Science 2012, 337:1658-1661.
46. Li H., Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010, 26:589-595.
47. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 1000 Genome Project Data Processing Subgroup.
48. Liao M., Cao E., Julius D., Cheng Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 2013, 504:107-112.
49. Liu S., Lorenzen E.D., Fumagalli M., Li B., Harris K., Xiong Z., Zhou L., Korneliussen T.S., Somel M., Babbitt C., et al. Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears. Cell 2014, 157:785-794.
50. Lu W., Meng Q.-J., Tyler N.J.C., Stokkan K.-A., Loudon A.S.I. A circadian clock is not required in an arctic mammal. Curr. Biol. 2010, 20:533-537.
51. MacDonald G.M., Beilman D.W., Kuzmin Y.V., Orlova L.A., Kremenetski K.V., Shapiro B., Wayne R.K., Van Valkenburgh B. Pattern of extinction of the woolly mammoth in Beringia. Nat. Commun. 2012, 3:893.
52. Mandadi S., Sokabe T., Shibasaki K., Katanosaka K., Mizuno A., Moqrich A., Patapoutian A., Fukumi-Tominaga T., Mizumura K., Tominaga M. TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pflugers Arch. 2009, 458:1093-1102.
53. Marics I., Malapert P., Reynders A., Gaillard S., Moqrich A. Acute heat-evoked temperature sensation is impaired but not abolished in mice lacking TRPV1 and TRPV3 channels. PLoS One 2014, 9:e99828.
54. Miller W., Drautz D.I., Ratan A., Pusey B., Qi J., Lesk A.M., Tomsho L.P., Packard M.D., Zhao F., Sher A., et al. Sequencing the nuclear genome of the extinct woolly mammoth. Nature 2008, 456:387-390.
55. Miyamoto T., Petrus M.J., Dubin A.E., Patapoutian A. TRPV3 regulates nitric oxide synthase-independent nitric oxide synthesis in the skin. Nat. Commun. 2011, 2:369.
56. Moqrich A., Hwang S.W., Earley T.J., Petrus M.J., Murray A.N., Spencer K.S., Andahazy M., Story G.M., Patapoutian A. Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 2005, 307:1468-1472.
57. Nelson O.L., Jansen H.T., Galbreath E., Morgenstern K., Gehring J.L., Rigano K.S., Lee J., Gong J., Shaywitz A.J., Vella C.A., et al. Grizzly bears exhibit augmented insulin sensitivity while obese prior to a reversible insulin resistance during hibernation. Cell Metab. 2014, 20:376-382.
58. Nielsen R. Mapping mutations on phylogenies. Syst. Biol. 2002, 51:729-739.
59. Paulsen C.E., Armache J.-P., Gao Y., Cheng Y., Julius D. Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 2015, 520:511-517.
60. Peier A.M., Reeve A.J., Andersson D.A., Moqrich A., Earley T.J., Hergarden A.C., Story G.M., Colley S., Hogenesch J.B., McIntyre P., et al. A heat-sensitive TRP channel expressed in keratinocytes. Science 2002, 296:2046-2049.
61. Pupko T., Pe'er I., Shamir R., Graur D. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol. Biol. Evol. 2000, 17:890-896.
62. Repin V.E., Taranov O.S., Ryabchikova, Tikhonov A.N., Pugachev V.G. Sebaceous glands of the woolly mammoth, Mammothus primigenius Blum: histological evidence. Dokl. Biol. Sci. 2004, 398:382-384.
63. Reubish D., Emerling D., Defalco J., Steiger D., Victoria C., Vincent F. Functional assessment of temperature-gated ion-channel activity using a real-time PCR machine. Biotechniques 2009, 47:iii-ix.
64. Rohland N., Malaspinas A.-S., Pollack J.L., Slatkin M., Matheus P., Hofreiter M. Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biol. 2007, 5:e207.
65. Römpler H., Rohland N., Lalueza-Fox C., Willerslev E., Kuznetsova T., Rabeder G., Bertranpetit J., Schöneberg T., Hofreiter M. Nuclear gene indicates coat-color polymorphism in mammoths. Science 2006, 313:62.
66. Roy A., Kucukural A., Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5:725-738.
67. Saini C., Morf J., Stratmann M., Gos P., Schibler U. Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators. Genes Dev. 2012, 26:567-580.
68. Shiromani P.J., Xu M., Winston E.M., Shiromani S.N., Gerashchenko D., Weaver D.R. Sleep rhythmicity and homeostasis in mice with targeted disruption of mPeriod genes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287:R47-R57.
69. Smith G.D., Gunthorpe M.J., Kelsell R.E., Hayes P.D., Reilly P., Facer P., Wright J.E., Jerman J.C., Walhin J.-P., Ooi L., et al. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 2002, 418:186-190.
70. Smith S.D., Wang S., Rausher M.D. Functional evolution of an anthocyanin pathway enzyme during a flower color transition. Mol. Biol. Evol. 2013, 30:602-612.
71. Storz J.F., Runck A.M., Sabatino S.J., Kelly J.K., Ferrand N., Moriyama H., Weber R.E., Fago A. Evolutionary and functional insights into the mechanism underlying high-altitude adaptation of deer mouse hemoglobin. Proc. Natl. Acad. Sci. USA 2009, 106:14450-14455.
72. Tang Z., Kim A., Masuch T., Park K., Weng H., Wetzel C., Dong X. Pirt functions as an endogenous regulator of TRPM8. Nat. Commun. 2013, 4:2179.
73. Toyota H., Dugovic C., Koehl M., Laposky A.D., Weber C., Ngo K., Wu Y., Lee D.H., Yanai K., Sakurai E., et al. Behavioral characterization of mice lacking histamine H(3) receptors. Mol. Pharmacol. 2002, 62:389-397.
74. Valente A. Hair structure of the Woolly mammoth, Mammuthus primigenius and the modern elephants, Elephas maximus and Loxodonta africana. J. Zool. 1983, 199:271-274.
75. Vandewauw I., Owsianik G., Voets T. Systematic and quantitative mRNA expression analysis of TRP channel genes at the single trigeminal and dorsal root ganglion level in mouse. BMC Neurosci. 2013, 14:21.
76. Vizin R.C.L., Scarpellini Cda.S., Ishikawa D.T., Correa G.M., de Souza C.O., Gargaglioni L.H., Carrettiero D.C., Bícego K.C., Almeida M.C. TRPV4 activates autonomic and behavioural warmth-defence responses in Wistar rats. Acta Physiol. (Oxf.) 2015, 214:275-289.
77. Vriens J., Nilius B., Voets T. Peripheral thermosensation in mammals. Nat. Rev. Neurosci. 2014, 15:573-589.
78. Workman C., Dalén L., Vartanyan S., Shapiro B., Kosintsev P., Sher A., Götherström A., Barnes I. Population-level genotyping of coat colour polymorphism in woolly mammoth (Mammuthus primigenius). Quat. Sci. Rev. 2011, 30:2304-2308.
79. Xu D., Zhang Y. Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophys. J. 2011, 101:2525-2534.
80. Xu H., Ramsey I.S., Kotecha S.A., Moran M.M., Chong J.A., Lawson D., Ge P., Lilly J., Silos-Santiago I., Xie Y., et al. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 2002, 418:181-186.
81. Yang Z., Kumar S., Nei M. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 1995, 141:1641-1650.
82. Yuan Y., Shen T.-J., Gupta P., Ho N.T., Simplaceanu V., Tam T.C.S., Hofreiter M., Cooper A., Campbell K.L., Ho C. A biochemical-biophysical study of hemoglobins from woolly mammoth, Asian elephant, and humans. Biochemistry 2011, 50:7350-7360.
83. Yuan Y., Byrd C., Shen T.-J., Simplaceanu V., Tam T.C.S., Ho C. Role of β/δ101Gln in regulating the effect of temperature and allosteric effectors on oxygen affinity in woolly mammoth hemoglobin. Biochemistry 2013, 52:8888-8897.
84. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 2008, 9:40.