Влияние породы и среды на длину теломер лейкоцитов у крупного рогатого скота

Высокие удои молока сопряжены с сокращением продолжительности жизни у высокопродуктивных молочных пород скота. Преждевременная выбраковка приводит к значительным экономическим потерям в молочном животноводстве и увеличению потребности в ремонтных телках. Отбор по этому признаку затруднен из-за низкой наследуемости и сложности измерения данного фенотипа. Теломеры – это структуры, находящиеся на концах хромосом, состоящие из повторяющихся последовательностей ДНК длиной в несколько тысяч пар оснований, связанных с нуклеопротеиновыми комплексами. У людей и большинства других животных длина теломер уменьшается с возрастом. Когда теломерная ДНК сокращается до критической длины, индуцируются процессы старения клеток, остановки клеточного цикла и апоптоза. В результате длину теломер можно рассматривать как предиктор рисков для здоровья и продолжительности жизни индивида. Длина теломер лейкоцитов может быть использована в качестве суррогатного фенотипа для признака продуктивного долголетия для улучшения селекции крупного рогатого скота. Целью нашей работы было – оценить влияние породы и направления продуктивности (молочное или мясное) на длину теломер лейкоцитов, а также проанализировать влияние холодного климата на этот признак в популяциях крупного рогатого скота калмыцкой породы на Юге (Ростовская область) и Крайнем Севере (Республика Саха) России. Измерение длины теломер лейкоцитов осуществлено с помощью компьютерных методов на основе данных полногеномного ресеквенирования. Мы использовали данные о длине теломер лейкоцитов, половой принадлежности и возрасте 239 животных, относящихся к 17 породам крупного рогатого скота. Фактор породы оказывает существенное влияние на длину теломер лейкоцитов в нашей выборке. Достоверных различий в длине теломер лейкоцитов между молочными и мясными группами нами не выявлено. Значительное влияние на длину теломер лейкоцитов у животных калмыцкой породы оказывает фактор популяции. Таким образом, мы обнаружили, что именно порода, но не направление продуктивности (молочное или мясное), достоверно влияла на длину теломер лейкоцитов у крупного рогатого скота. Разведение в более холодном климате было ассоциировано с большей длиной теломер лейкоцитов у крупного рогатого скота калмыцкой породы.

1. Andrew T., Aviv A., Falchi M., Surdulescu G.L., Gardner J.P., Lu X., Kimura M., Kato B.S., Valdes A.M., Spector T.D. Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. Am. J. Hum. Genet. 2006;78(3): 480-486. DOI 10.1086/500052

2. Armanios M. The role of telomeres in human disease. Annu. Rev. Genomics Hum. Genet. 2022;23:363-381. DOI 10.1146/annurev- genom-010422-091101

3. Asghar M., Palinauskas V., Zaghdoudi-Allan N., Valkiūnas G., Mukhin A., Platonova E., Färnert A., Bensch S., Hasselquist D. Parallel telomere shortening in multiple body tissues owing to malaria infection. Proc. Biol. Sci. 2016;283(1836):20161184. DOI 10.1098/ rspb.2016.1184

4. Astuti Y., Wardhana A., Watkins J., Wulaningsih W.; PILAR Research Network. Cigarette smoking and telomere length: A systematic review of 84 studies and meta-analysis. Environ. Res. 2017;158:480-

5. DOI 10.1016/j.envres.2017.06.038

6. Behr A.A., Liu K.Z., Liu-Fang G., Nakka P., Ramachandran S. pong: fast analysis and visualization of latent clusters in population genetic data. Bioinformatics. 2016;32(18):2817-2823. DOI 10.1093/ bioinformatics/btw327

7. Ben-Shachar M.S., Lüdecke D., Makowski D. effectsize: Estimation of effect size indices and standardized parameters. J. Open Source

8. Softw. 2020;5(56):2815. DOI 10.21105/joss.02815

9. Blackburn E.H., Epel E.S., Lin J. Human telomere biology: A contributory and interactive factor in aging, disease risks, and protection. Science. 2015;350(6265):1193-1198. DOI 10.1126/science.aab3389

10. Broer L., Codd V., Nyholt D.R., Deelen J., Mangino M., Willemsen G., Albrecht E., … Vink J.M., Spector T.D., Slagboom P.E., Martin N.G., Samani N.J., van Duijn C.M., Boomsma D.I. Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur. J. Hum.

11. Genet. 2013;21(10):1163-1168. DOI 10.1038/ejhg.2012.303

12. Brown D.E., Dechow C.D., Liu W.S., Harvatine K.J., Ott T.L. Hot topic: association of telomere length with age, herd, and culling in lactating Holsteins. J. Dairy Sci. 2012;95(11):6384-6387. DOI 10.3168/jds.2012-5593

13. Burraco P., Hernandez-Gonzalez M., Metcalfe N.B., Monaghan P. Ageing across the great divide: tissue transformation, organismal growth and temperature shape telomere dynamics through the metamorphic transition. Proc. Biol. Sci. 2023;290(1992):20222448. DOI 10.1098/rspb.2022.2448

14. Carrillo A.E., Flouris A.D. Caloric restriction and longevity: effects of reduced body temperature. Ageing Res. Rev. 2011;10(1):153-162. DOI 10.1016/j.arr.2010.10.001

15. Chakravarti D., LaBella K.A., DePinho R.A. Telomeres: history, health, and hallmarks of aging. Cell. 2021;184(2):306-322. DOI 10.1016/ j.cell.2020.12.028

16. Chatelain M., Drobniak S.M., Szulkin M. The association between stressors and telomeres in non-human vertebrates: a meta-analysis.

17. Ecol. Lett. 2020;23(2):381-398. DOI 10.1111/ele.13426

18. Chik H.Y.J., Sparks A.M., Schroeder J., Dugdale H.L. A meta-analysis on the heritability of vertebrate telomere length. J. Evol. Biol.

19. ;35(10):1283-1295. DOI 10.1111/jeb.14071

20. Conti B., Sanchez-Alavez M., Winsky-Sommerer R., Morale M.C., Lucero J., Brownell S., Fabre V., Huitron-Resendiz S., Henriksen S., Zorrilla E.P., de Lecea L., Bartfai T. Transgenic mice with a reduced core body temperature have an increased life span. Science. 2006;

21. (5800):825-828. DOI 10.1126/science.1132191

22. Cook D.E., Zdraljevic S., Tanny R.E., Seo B., Riccardi D.D., Noble L.M., Rockman M.V., Alkema M.J., Braendle C., Kammenga J.E., Wang J., Kruglyak L., Félix M.A., Lee J., Andersen E.C. The genetic basis of natural variation in Caenorhabditis elegans telomere length. Genetics. 2016;204(1):371-383. DOI 10.1534/genetics.116. 191148

23. Crocco P., De Rango F., Dato S., Rose G., Passarino G. Telomere length as a function of age at population level parallels human survival curves. Aging (Albany NY ). 2021;13(1):204-218. DOI 10.18632/ aging.202498

24. de Lange T. Shelterin-mediated telomere protection. Annu. Rev. Genet. 2018;52:223-247. DOI 10.1146/annurev-genet-032918-021921

25. Ding Z., Mangino M., Aviv A., Spector T., Durbin R. Estimating telomere length from whole genome sequence data. Nucleic Acids Res. 2014;42(9):e75. DOI 10.1093/nar/gku181

26. Dmitriev N.G., Ernst L.K. (Eds.). Animal Genetics Resources of the USSR. Rome: Food and Agriculture Organization of the United Nations, 1989

27. Dugdale H.L., Richardson D.S. Heritability of telomere variation: it is all about the environment! Philos. Trans. R. Soc. Lond. B Biol. Sci. 2018;373(1741):20160450. DOI 10.1098/rstb.2016.0450

28. Dunin I.M., Dankvert A.G. (Eds.). Breeds and Types of Farm Animals in the Russian Federation. Moscow: All-Russia Research Institute of Animal Breeding, 2013 (in Russian)

29. Fick L.J., Fick G.H., Li Z., Cao E., Bao B., Heffelfinger D., Parker H.G., Ostrander E.A., Riabowol K. Telomere length correlates with life span of dog breeds. Cell Rep. 2012;2(6):1530-1536. DOI

30. 1016/j.celrep.2012.11.021

31. Foley N.M., Petit E.J., Brazier T., Finarelli J.A., Hughes G.M., Touzalin F., Puechmaille S.J., Teeling E.C. Drivers of longitudinal telomere dynamics in a long-lived bat species, Myotis myotis. Mol. Ecol. 2020;29(16):2963-2977. DOI 10.1111/mec.15395

32. Friesen C.R., Wapstra E., Olsson M. Of telomeres and temperature: Measuring thermal effects on telomeres in ectothermic animals. Mol.

33. Ecol. 2022;31(23):6069-6086. DOI 10.1111/mec.16154

34. Fulbert C., Gaude C., Sulpice E., Chabardès S., Ratel D. Moderate hypothermia inhibits both proliferation and migration of human glioblastoma cells. J. Neurooncol. 2019;144(3):489-499. DOI 10.1007/

35. s11060-019-03263-3

36. Galigniana N.M., Charó N.L., Uranga R., Cabanillas A.M., Piwien-Pilipuk G. Oxidative stress induces transcription of telomeric repeatcontaining RNA (TERRA) by engaging PKA signaling and cytoskeleton dynamics. Biochim. Biophys. Acta Mol. Cell. Res. 2020; 1867(4):118643. DOI 10.1016/j.bbamcr.2020.118643

37. Grandl F., Furger M., Kreuzer M., Zehetmeier M. Impact of longev ity on greenhouse gas emissions and profitability of individual dairy cows analysed with different system boundaries. Animal. 2019; 13(1):198-208. DOI 10.1017/S175173111800112X

38. Herborn K.A., Heidinger B.J., Boner W., Noguera J.C., Adam A., Daunt F., Monaghan P. Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. Proc. Biol. Sci. 2014;281(1782):20133151. DOI 10.1098/ rspb.2013.3151

39. Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom. J. 2008;50(3):346-363. DOI 10.1002/ bimj.20081042

40. Hu H., Mu T., Ma Y., Wang X., Ma Y. Analysis of longevity traits in Holstein cattle: A review. Front. Genet. 2021;12:695543. DOI

41. 3389/fgene.2021.695543

42. Iannuzzi A., Albarella S., Parma P., Galdiero G., D’Anza E., Pistucci R., Peretti V., Ciotola F. Characterization of telomere length in Agerolese cattle breed, correlating blood and milk samples. Anim.

43. Genet. 2022;53(5):676-679. DOI 10.1111/age.13227

44. Igoshin A.V., Yudin N.S., Romashov G.A., Larkin D.M. A multibreed genome-wide association study for cattle leukocyte telomere length. Genes (Basel). 2023;14(8):1596. DOI 10.3390/ genes14081596

45. Ilska-Warner J.J., Psifidi A., Seeker L.A., Wilbourn R.V., Underwood S.L., Fairlie J., Whitelaw B., Nussey D.H., Coffey M.P., Banos G. The genetic architecture of bovine telomere length in early life and association with animal fitness. Front. Genet. 2019;10: 1048. DOI 10.3389/fgene.2019.01048

46. Jenner L.P., Peska V., Fulnečková J., Sýkorová E. Telomeres and their neighbors. Genes (Basel). 2022;13(9):1663. DOI 10.3390/genes130

47.

48. Kanagawa T., Fukuda H., Tsubouchi H., Komoto Y., Hayashi S., Fukui O., Shimoya K., Murata Y. A decrease of cell proliferation by hypothermia in the hippocampus of the neonatal rat. Brain Res.

49. ;1111(1):36-40. DOI 10.1016/j.brainres.2006.06.112

50. Kayumov F.G., Chernomyrdin V.N., Mayevskaya L.A., Surundaeva L.G., Polskikh S.S. The use of Kalmyk cattle on animal breeding farms in Russia. Izv. Orenbg. State Agrar. Univ. 2014;5(49):116-119

51. (in Russian)

52. Kordowitzki P., Merle R., Hass P.-K., Plendl J., Rieger J., Kaessmeyer S. Influence of age and breed on bovine ovarian capillary blood supply, ovarian mitochondria and telomere length. Cells.

53. ;10(10):2661. DOI 10.3390/cells10102661

54. Lantz B. The impact of sample non-normality on ANOVA and alternative methods. Br. J. Math. Stat. Psychol. 2013;66(2):224-244. DOI

55. 1111/j.2044-8317.2012.02047.x

56. Laubenthal L., Hoelker M., Frahm J., Dänicke S., Gerlach K., Südekum K.-H., Sauerwein H., Häussler S. Short communication: Telomere lengths in different tissues of dairy cows during early and late lactation. J. Dairy Sci. 2016;99(6):4881-4885. DOI 10.3168/jds.

57. -10095

58. Law E., Girgis A., Lambert S., Sylvie L., Levesque J., Pickett H. Telomeres and stress: promising avenues for research in psycho-oncology. Asia-Pacific J. Oncol. Nurs. 2016;3(2):137-147. DOI 10.4103/ 2347-5625.182931

59. Leung C.W., Laraia B.A., Needham B.L., Rehkopf D.H., Adler N.E., Lin J., Blackburn E.H., Epel E.S. Soda and cell aging: associations between sugar-sweetened beverage consumption and leukocyte telomere length in healthy adults from the National Health and Nutrition

60. Examination Surveys. Am. J. Public Health. 2014;104(12):2425-

61. DOI 10.2105/AJPH.2014.302151

62. Lhasaranov B. Pasture animal husbandry in Eastern Siberia. Biomed. J. Sci. Tech. Res. 2020;31(3):24160-24163. DOI 10.26717/BJSTR. 2020.31.005094

63. Lin J., Epel E. Stress and telomere shortening: Insights from cellular mechanisms. Ageing Res. Rev. 2022;73:101507. DOI 10.1016/j.arr. 2021.101507

64. Liu J., Wang L., Wang Z., Liu J.-P. Roles of telomere biology in cell senescence, replicative and chronological ageing. Cells. 2019;8(1): 54. DOI 10.3390/cells8010054

65. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G.

66. Hallmarks of aging: An expanding universe. Cell. 2023;186(2):243278. DOI 10.1016/j.cell.2022.11.001

67. Lynch S.M., Peek M.K., Mitra N., Ravichandran K., Branas C., Spangler E., Zhou W., Paskett E.D., Gehlert S., DeGraffinreid C., Rebbeck T.R., Riethman H. Race, ethnicity, psychosocial factors, and telomere length in a multicenter setting. PLoS One. 2016;11(1): e0146723. DOI 10.1371/journal.pone.0146723

68. Manning E.L., Crossland J., Dewey M.J., Van Zant G. Influences of inbreeding and genetics on telomere length in mice. Mamm. Genome.

69. ;13(5):234-238. DOI 10.1007/s003350020027

70. Martens D.S., Plusquin M., Cox B., Nawrot T.S. Early biological aging and fetal exposure to high and low ambient temperature: A birth cohort study. Environ. Health Perspect. 2019;127(11):117001. DOI 10.1289/EHP5153

71. McLennan D., Armstrong J.D., Stewart D.C., Mckelvey S., Boner W., Monaghan P., Metcalfe N.B. Telomere elongation during early development is independent of environmental temperatures in Atlantic salmon. J. Exp. Biol. 2018;221(Pt. 11):jeb178616. DOI 10.1242/ jeb.178616

72. Meesters M., Van Eetvelde M., Martens D.S., Nawrot T.S., Dewulf M., Govaere J., Opsomer G. Prenatal environment impacts telomere length in newborn dairy heifers. Sci. Rep. 2023;13(1):4672. DOI

73. 1038/s41598-023-31943-8

74. Miyashita N., Shiga K., Yonai M., Kaneyama K., Kobayashi S., Kojima T., Goto Y., Kishi M., Aso H., Suzuki T., Sakaguchi M., Nagai T. Remarkable differences in telomere lengths among cloned cattle derived from different cell types. Biol. Reprod. 2002;66(6):1649-1655. DOI 10.1095/biolreprod66.6.1649

75. Mizutani Y., Niizuma Y., Yoda K. How do growth and sibling competition affect telomere dynamics in the first month of life of long-lived seabird? PLoS One. 2016;11(11):e0167261. DOI 10.1371/journal. pone.0167261

76. Monaghan P., Ozanne S.E. Somatic growth and telomere dynamics in vertebrates: relationships, mechanisms and consequences. Philos. Trans. R. Soc. London Ser. B. Biol. Sci. 2018;373(1741):20160446.

77. DOI 10.1098/rstb.2016.0446

78. Nowack J., Tarmann I., Hoelzl F., Smith S., Giroud S., Ruf T. Always a price to pay: hibernation at low temperatures comes with a trade-off between energy savings and telomere damage. Biol. Lett. 2019;15(10):20190466. DOI 10.1098/rsbl.2019.0466

79. O’Daniel S.E., Kochan K.J., Long C.R., Riley D.G., Randel R.D., Welsh T.H.J. Comparison of telomere length in age-matched primiparous and multiparous Brahman cows. Animals (Basel). 2023; 13(14):2325. DOI 10.3390/ani13142325

80. Pinese M., Lacaze P., Rath E.M., Stone A., Brion M.-J., Ameur A., Nagpal S., … Kaplan W., Gibson G., Gyllensten U., Cairns M.J.,

81. McNamara M., Dinger M.E., Thomas D.M. The Medical Genome Reference Bank contains whole genome and phenotype data of 2570 healthy elderly. Nat. Commun. 2020;11(1):435. DOI 10.1038/

82. s41467-019-14079-0

83. Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A.R., Bender D., Maller J., Sklar P., de Bakker P.I.W., Daly M.J., Sham P.C. PLINK: a tool set for whole-genome association and populationbased linkage analyses. Am. J. Hum. Genet. 2007;81(3):559-575. DOI 10.1086/519795

84. Rafie N., Golpour Hamedani S., Barak F., Safavi S.M., Miraghajani M. Dietary patterns, food groups and telomere length: a systematic review of current studies. Eur. J. Clin. Nutr. 2017;71(2):151-158. DOI 10.1038/ejcn.2016.149

85. Raj A., Stephens M., Pritchard J.K. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics. 2014;197(2):573-589. DOI 10.1534/genetics.114.164350

86. Reichert S., Stier A., Zahn S., Arrivé M., Bize P., Massemin S., Criscuolo F. Increased brood size leads to persistent eroded telomeres. Front. Ecol. Evol. 2014;2:9. DOI 10.3389/fevo.2014.00009

87. Ribas-Maynou J., Llavanera M., Mateo-Otero Y., Ruiz N., Muiño R., Bonet S., Yeste M. Telomere length in bovine sperm is related to the production of reactive oxygen species, but not to reproductive performance. Theriogenology. 2022;189:290-300. DOI 10.1016/ j.theriogenology.2022.06.025

88. Rossiello F., Jurk D., Passos J.F., d’Adda di Fagagna F. Telomere dysfunction in ageing and age-related diseases. Nat. Cell Biol. 2022; 24(2):135-147. DOI 10.1038/s41556-022-00842-x

89. Schrumpfová P.P., Fajkus J. Composition and function of telomerase-A polymerase associated with the origin of eukaryotes. Biomolecules. 2020;10(10):1425. DOI 10.3390/biom10101425

90. Seeker L.A., Ilska J.J., Psifidi A., Wilbourn R.V., Underwood S.L., Fairlie J., Holland R., Froy H., Salvo-Chirnside E., Bagnall A., Whitelaw B., Coffey M.P., Nussey D.H., Banos G. Bovine telomere dynamics and the association between telomere length and productive lifespan. Sci. Rep. 2018a;8(1):12748. DOI 10.1038/s41598-018-

91. -z

92. Seeker L.A., Ilska J.J., Psifidi A., Wilbourn R.V., Underwood S.L., Fairlie J., Holland R., Froy H., Bagnall A., Whitelaw B., Coffey M., Nussey D.H., Banos G. Longitudinal changes in telomere length and associated genetic parameters in dairy cattle analysed using random regression models. PLoS One. 2018b;13(2):e0192864. DOI

93. 1371/journal.pone.0192864

94. Seeker L.A., Underwood S.L., Wilbourn R.V., Dorrens J., Froy H., Holland R., Ilska J.J., Psifidi A., Bagnall A., Whitelaw B., Coffey M., Banos G., Nussey D.H. Telomere attrition rates are associated with weather conditions and predict productive lifespan in dairy cattle.

95. Sci. Rep. 2021;11(1):5589. DOI 10.1038/s41598-021-84984-2

96. Sleptsov I.I., Machakhtyrova V.A., Ivanova N.P. Clinical and physiological indicators of the Kalmyk cattle breed in Yakutia conditions. Bull. Kurgan State Agric. Acad. 2019;4(32):44-46 (in Russian)

97. Szczotka M., Kocki J., Iwan E., Pluta A. Determination of telomere length and telomerase activity in cattle infected with bovine leukaemia virus (BLV). Pol. J. Vet. Sci. 2019;22(2):391-403. DOI 10.24425/pjvs.2019.129299

98. Taub M.A., Conomos M.P., Keener R., Iyer K.R., Weinstock J.S., Yanek L.R., Lane J., … de Andrade M., Correa A., Chen Y.I., Boerwinkle E., Barnes K.C., Ashley-Koch A.E., Arnett D.K.; NHLBI Trans-Omics for Precision Medicine (TOPMed) Consortium; TOPMed Hematology and Hemostasis Working Group; TOPMed

99. Structural Variation Working Group; Laurie C.C., Abecasis G., Nickerson D.A., Wilson J.G., Rich S.S., Levy D., Ruczinski I., Aviv A., Blackwell T.W., Thornton T., O’Connell J., Cox N.J., Perry J.A., Armanios M., Battle A., Pankratz N., Reiner A.P., Mathias R.A. Genetic determinants of telomere length from 109,122 ancestrally diverse whole-genome sequences in TOPMed. Cell Genom.

100. ;2(1):100084. DOI 10.1016/j.xgen.2021.100084

101. Tilesi F., Di Domenico E.G., Pariset L., Bosco L., Willems D., Valentini A., Ascenzioni F. Telomere length diversity in cattle breeds. Diversity. 2010;2(9):1118-1129. DOI 10.3390/d2091118

102. Waalen J., Buxbaum J.N. Is older colder or colder older? The association of age with body temperature in 18,630 individuals. J. Gerontol. A Biol. Sci. Med. Sci. 2011;66(5):487-492. DOI 10.1093/gerona/ glr001

103. Whittemore K., Vera E., Martínez-Nevado E., Sanpera C., Blasco M.A. Telomere shortening rate predicts species life span. Proc. Natl. Acad. Sci. USA. 2019;116(30):15122-15127. DOI 10.1073/pnas. 1902452116

104. Wilbourn R.V., Moatt J.P., Froy H., Walling C.A., Nussey D.H., Boonekamp J.J. The relationship between telomere length and mortality risk in non-model vertebrate systems: a meta-analysis. Philos. Trans. R. Soc. London Ser. B. Biol. Sci. 2018;373(1741):20160447. DOI 10.1098/rstb.2016.0447

105. Zepner L., Karrasch P., Wiemann F., Bernard L. ClimateCharts.net – an interactive climate analysis web platform. Int. J. Digit. Earth. 2021; 14(3):338-356. DOI 10.1080/17538947.2020.1829112

106. Zhang D., Newton C.A., Wang B., Povysil G., Noth I., Martinez F.J., Raghu G., Goldstein D., Garcia C.K. Utility of whole genome sequencing in assessing risk and clinically relevant outcomes for pulmonary fibrosis. Eur. Respir. J. 2022;60(6):2200577. DOI 10.1183/ 13993003.00577-2022

107. Zhang H., Liu A., Wang Y., Luo H., Yan X., Guo X., Li X., Liu L., Su G. Genetic parameters and genome-wide association studies of eight longevity traits representing either full or partial lifespan in Chinese Holsteins. Front. Genet. 2021;12:634986. DOI 10.3389/ fgene.2021.634986

108. Zhang X., Lin S., Funk W.E., Hou L. Environmental and occupational exposure to chemicals and telomere length in human studies. Occup. Environ. Med. 2013;70(10):743-749. DOI 10.1136/

109. oemed-2012-101350

110. Zhang Y., Wu Y., Mao P., Li F., Han X., Zhang Y., Jiang S., Chen Y., Huang J., Liu D., Zhao Y., Ma W., Songyang Z. Cold-inducible RNAbinding protein CIRP/hnRNP A18 regulates telomerase activity in a temperature-dependent manner. Nucleic Acids Res. 2016;44(2):

111. -775. DOI 10.1093/nar/gkv1465

112. Zhao Z., Cao J., Niu C., Bao M., Xu J., Huo D., Liao S., Liu W., Speakman J.R. Body temperature is a more important modulator of lifespan than metabolic rate in two small mammals. Nat. Metab. 2022; 4(3):320-326. DOI 10.1038/s42255-022-00545-5