Syndecan-1 Is Required to Maintain Intradermal Fat and Prevent Cold Stress

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All mammals strive to maintain a fixed body temperature, and do so using a remarkable array of different strategies, which vary depending upon the degree of cold challenge. Physiologists many decades ago observed that a fat layer right underneath the epidermis (and above the dermal muscle layer) thickens in response to colder ambient temperatures. This “intradermal fat” provided insulation within days of climate changes. We have found that syndecan-1, which functions as a facultative lipoprotein uptake receptor, is required for intradermal fat expansion in response to cold exposure. This is a highly specific phenotype not shared by other adipocytes. When intradermal fat is absent, mice do not adapt normally to cold stress, and show altered systemic physiologies, including increased brown adipose tissue thermogenesis and hyper-activation of a stress checkpoint (p38α), designed to protect the body against mutagenic and oxidative stressors. The phenotypes associated with loss of Sdc1 function are reversed when mice are housed in warm temperatures, where defense of body temperature is not required. This study is the first to show that intradermal fat can be genetically regulated, with systemic effects on physiology.

Vyšlo v časopise: Syndecan-1 Is Required to Maintain Intradermal Fat and Prevent Cold Stress. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004514
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004514

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Zdroje

1. KarpCL (2012) Unstressing intemperate models: how cold stress undermines mouse modeling. The Journal of experimental medicine 209: 1069–1074.

2. GolozoubovaV, GullbergH, MatthiasA, CannonB, VennstromB, et al. (2004) Depressed thermogenesis but competent brown adipose tissue recruitment in mice devoid of all hormone-binding thyroid hormone receptors. Molecular endocrinology 18: 384–401.

3. OvertonJM, WilliamsTD (2004) Behavioral and physiologic responses to caloric restriction in mice. Physiology & behavior 81: 749–754.

4. GordonCJ (2012) Thermal physiology of laboratory mice: Defining thermoneutrality. Journal of Thermal Biology 37: 654–685.

5. NguyenKD, QiuY, CuiX, GohYP, MwangiJ, et al. (2011) Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 480: 104–108.

6. CannonB, NedergaardJ (2004) Brown adipose tissue: function and physiological significance. Physiological reviews 84: 277–359.

7. JordtSE, McKemyDD, JuliusD (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Current opinion in neurobiology 13: 487–492.

8. KozakLP (2011) The genetics of brown adipocyte induction in white fat depots. Frontiers in endocrinology 2: 64.

9. YeL, WuJ, CohenP, KazakL, KhandekarMJ, et al. (2013) Fat cells directly sense temperature to activate thermogenesis. Proceedings of the National Academy of Sciences of the United States of America 110: 12480–12485.

10. KajimuraS, SealeP, SpiegelmanBM (2010) Transcriptional control of brown fat development. Cell metabolism 11: 257–262.

11. KokolusKM, CapitanoML, LeeCT, EngJW, WaightJD, et al. (2013) Baseline tumor growth and immune control in laboratory mice are significantly influenced by subthermoneutral housing temperature. Proceedings of the National Academy of Sciences of the United States of America doi: 10.1073/pnas.1304291110

12. FeldmannHM, GolozoubovaV, CannonB, NedergaardJ (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell metabolism 9: 203–209.

13. RapraegerAC (2001) Molecular interactions of syndecans during development. Seminars in cell & developmental biology 12: 107–116.

14. CouchmanJR (2010) Transmembrane signaling proteoglycans. Annual review of cell and developmental biology 26: 89–114.

15. BernfieldM, GotteM, ParkPW, ReizesO, FitzgeraldML, et al. (1999) Functions of cell surface heparan sulfate proteoglycans. Annual review of biochemistry 68: 729–777.

16. McDermottSP, RanheimEA, LeatherberryVS, KhwajaSS, KlosKS, et al. (2007) Juvenile syndecan-1 null mice are protected from carcinogen-induced tumor development. Oncogene 26: 1407–1416.

17. AlexanderCM, ReichsmanF, HinkesMT, LincecumJ, BeckerKA, et al. (2000) Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nature Genetics 25: 329–332.

18. TengYH, AquinoRS, ParkPW (2012) Molecular functions of syndecan-1 in disease. Matrix biology : journal of the International Society for Matrix Biology 31: 3–16.

19. StanfordKI, BishopJR, FoleyEM, GonzalesJC, NiesmanIR, et al. (2009) Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. The Journal of clinical investigation 119: 3236–3245.

20. StanfordKI, WangL, CastagnolaJ, SongD, BishopJR, et al. (2010) Heparan sulfate 2-O-sulfotransferase is required for triglyceride-rich lipoprotein clearance. The Journal of biological chemistry 285: 286–294.

21. ReshefL, OlswangY, CassutoH, BlumB, CronigerCM, et al. (2003) Glyceroneogenesis and the triglyceride/fatty acid cycle. The Journal of biological chemistry 278: 30413–30416.

22. BarteltA, BrunsOT, ReimerR, HohenbergH, IttrichH, et al. (2011) Brown adipose tissue activity controls triglyceride clearance. Nature medicine 17: 200–205.

23. SwoapSJ (2008) The pharmacology and molecular mechanisms underlying temperature regulation and torpor. Biochemical pharmacology 76: 817–824.

24. GeiserF (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annual review of physiology 66: 239–274.

25. KliewerSA, MangelsdorfDJ (2010) Fibroblast growth factor 21: from pharmacology to physiology. The American journal of clinical nutrition 91: 254S–257S.

26. CaoW, DanielKW, RobidouxJ, PuigserverP, MedvedevAV, et al. (2004) p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol Cell Biol 24: 3057–3067.

27. CollinsS, BordicchiaM (2013) Heart hormones fueling a fire in fat. Adipocyte 2: 104–108.

28. BordicchiaM, LiuD, AmriEZ, AilhaudG, Dessi-FulgheriP, et al. (2012) Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. The Journal of clinical investigation 122: 1022–1036.

29. BirerdincA, JarrarM, StotishT, RandhawaM, BaranovaA (2013) Manipulating molecular switches in brown adipocytes and their precursors: a therapeutic potential. Progress in lipid research 52: 51–61.

30. GolozoubovaV, CannonB, NedergaardJ (2006) UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. Am J Physiol Endocrinol Metab 291: E350–357.

31. MineoPM, CassellEA, RobertsME, SchaefferPJ (2012) Chronic cold acclimation increases thermogenic capacity, non-shivering thermogenesis and muscle citrate synthase activity in both wild-type and brown adipose tissue deficient mice. Comparative biochemistry and physiology Part A, Molecular & integrative physiology 161: 395–400.

32. HaasB, MayerP, JennissenK, ScholzD, Berriel DiazM, et al. (2009) Protein kinase G controls brown fat cell differentiation and mitochondrial biogenesis. Science signaling 2: ra78.

33. KozakLP (2014) Genetic variation in brown fat activity and body weight regulation in mice: lessons for human studies. Biochimica et biophysica acta 1842: 370–376.

34. WuZ, PuigserverP, AnderssonU, ZhangC, AdelmantG, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115–124.

35. LehmanJJ, BargerPM, KovacsA, SaffitzJE, MedeirosDM, et al. (2000) Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. The Journal of clinical investigation 106: 847–856.

36. TvrdikP, AsadiA, KozakLP, NedergaardJ, CannonB, et al. (1997) Cig30, a mouse member of a novel membrane protein gene family, is involved in the recruitment of brown adipose tissue. The Journal of biological chemistry 272: 31738–31746.

37. CannonB, NedergaardJ (2011) Nonshivering thermogenesis and its adequate measurement in metabolic studies. J Exp Biol 214: 242–253.

38. NagyTR, ClairAL (2000) Precision and accuracy of dual-energy X-ray absorptiometry for determining in vivo body composition of mice. Obesity research 8: 392–398.

39. HansenLS, CoggleJE, WellsJ, CharlesMW (1984) The influence of the hair cycle on the thickness of mouse skin. The Anatomical record 210: 569–573.

40. FestaE, FretzJ, BerryR, SchmidtB, RodehefferM, et al. (2011) Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146: 761–771.

41. TschopMH, SpeakmanJR, ArchJR, AuwerxJ, BruningJC, et al. (2012) A guide to analysis of mouse energy metabolism. Nature methods 9: 57–63.

42. HuangC, MaWY, MaxinerA, SunY, DongZ (1999) p38 kinase mediates UV-induced phosphorylation of p53 protein at serine 389. The Journal of biological chemistry 274: 12229–12235.

43. WagnerEF, NebredaAR (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nature reviews Cancer 9: 537–549.

44. GuillouH, ZadravecD, MartinPG, JacobssonA (2010) The key roles of elongases and desaturases in mammalian fatty acid metabolism: Insights from transgenic mice. Progress in lipid research 49: 186–199.

45. YuFX, GuanKL (2013) The Hippo pathway: regulators and regulations. Genes & development 27: 355–371.

46. SpeakmanJR (2013) Measuring energy metabolism in the mouse - theoretical, practical, and analytical considerations. Frontiers in physiology 4: 34.

47. KaiyalaKJ, SchwartzMW (2011) Toward a more complete (and less controversial) understanding of energy expenditure and its role in obesity pathogenesis. Diabetes 60: 17–23.

48. ButlerAA, KozakLP (2010) A recurring problem with the analysis of energy expenditure in genetic models expressing lean and obese phenotypes. Diabetes 59: 323–329.

49. MacArthurJM, BishopJR, StanfordKI, WangL, BensadounA, et al. (2007) Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. The Journal of clinical investigation 117: 153–164.

50. LinX, YueP, ChenZ, SchonfeldG (2005) Hepatic triglyceride contents are genetically determined in mice: results of a strain survey. American journal of physiology Gastrointestinal and liver physiology 288: G1179–1189.

51. AlexanderJ, ChangGQ, DourmashkinJT, LeibowitzSF (2006) Distinct phenotypes of obesity-prone AKR/J, DBA2J and C57BL/6J mice compared to control strains. International journal of obesity 30: 50–59.

52. WilsieLC, GonzalesAM, OrlandoRA (2006) Syndecan-1 mediates internalization of apoE-VLDL through a low density lipoprotein receptor-related protein (LRP)-independent, non-clathrin-mediated pathway. Lipids in health and disease 5: 23.

53. ReizesO, GoldbergerO, SmithAC, XuZ, BernfieldM, et al. (2006) Insulin promotes shedding of syndecan ectodomains from 3T3-L1 adipocytes: a proposed mechanism for stabilization of extracellular lipoprotein lipase. Biochemistry 45: 5703–5711.

54. FarmerSR (2006) Transcriptional control of adipocyte formation. Cell metabolism 4: 263–273.

55. TontonozP, SpiegelmanBM (2008) Fat and beyond: the diverse biology of PPARgamma. Annual review of biochemistry 77: 289–312.

56. CristanchoAG, LazarMA (2011) Forming functional fat: a growing understanding of adipocyte differentiation. Nature reviews Molecular cell biology 12: 722–734.

57. MoriH, PrestwichTC, ReidMA, LongoKA, GerinI, et al. (2012) Secreted frizzled-related protein 5 suppresses adipocyte mitochondrial metabolism through WNT inhibition. The Journal of clinical investigation 122: 2405–2416.

58. RimJS, MynattRL, Gawronska-KozakB (2005) Mesenchymal stem cells from the outer ear: a novel adult stem cell model system for the study of adipogenesis. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 19: 1205–1207.

59. ChenY, SiegelF, KipschullS, HaasB, FrohlichH, et al. (2013) miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit. Nature communications 4: 1769.

60. BrownJD, PlutzkyJ (2007) Peroxisome proliferator-activated receptors as transcriptional nodal points and therapeutic targets. Circulation 115: 518–533.

61. WuM, MelichianDS, ChangE, Warner-BlankenshipM, GhoshAK, et al. (2009) Rosiglitazone abrogates bleomycin-induced scleroderma and blocks profibrotic responses through peroxisome proliferator-activated receptor-gamma. The American journal of pathology 174: 519–533.

62. ScholanderPF, HockR, WaltersV, IrvingL (1950) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. The Biological bulletin 99: 259–271.

63. BarnettSA (1959) The skin and hair of mice living at a low environmental temperature. Quarterly journal of experimental physiology and cognate medical sciences 44: 35–42.

64. GaskillBN, GordonCJ, PajorEA, LucasJR, DavisJK, et al. (2013) Impact of nesting material on mouse body temperature and physiology. Physiology & Behavior 110: 87–95.

65. BeaudryJL, McClellandGB (2010) Thermogenesis in CD-1 mice after combined chronic hypoxia and cold acclimation. Comparative biochemistry and physiology Part B, Biochemistry & molecular biology 157: 301–309.

66. LeeSH, DobrzynA, DobrzynP, RahmanSM, MiyazakiM, et al. (2004) Lack of stearoyl-CoA desaturase 1 upregulates basal thermogenesis but causes hypothermia in a cold environment. Journal of lipid research 45: 1674–1682.

67. SampathH, NtambiJM (2011) The role of fatty acid desaturases in epidermal metabolism. Dermato-endocrinology 3: 62–64.

68. KharitonenkovA, ShiyanovaTL, KoesterA, FordAM, MicanovicR, et al. (2005) FGF-21 as a novel metabolic regulator. The Journal of clinical investigation 115: 1627–1635.

69. StratikopoulosE, SzabolcsM, DragatsisI, KlinakisA, EfstratiadisA (2008) The hormonal action of IGF1 in postnatal mouse growth. Proceedings of the National Academy of Sciences of the United States of America 105: 19378–19383.

70. PiedrahitaJA, ZhangSH, HagamanJR, OliverPM, MaedaN (1992) Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 89: 4471–4475.

71. SealeP, ConroeHM, EstallJ, KajimuraS, FrontiniA, et al. (2011) Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. The Journal of clinical investigation 121: 96–105.

72. BarbatelliG, MuranoI, MadsenL, HaoQ, JimenezM, et al. (2010) The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. American journal of physiology Endocrinology and metabolism 298: E1244–1253.

73. BarteltA, MerkelM, HeerenJ (2012) A new, powerful player in lipoprotein metabolism: brown adipose tissue. Journal of molecular medicine 90: 887–893.

74. BlanpainC, FuchsE (2006) Epidermal stem cells of the skin. Annual review of cell and developmental biology 22: 339–373.

75. ChiWY, Enshell-SeijffersD, MorganBA (2010) De novo production of dermal papilla cells during the anagen phase of the hair cycle. The Journal of investigative dermatology 130: 2664–2666.

76. RobidouxJ, CaoW, QuanH, DanielKW, MoukdarF, et al. (2005) Selective activation of mitogen-activated protein (MAP) kinase kinase 3 and p38alpha MAP kinase is essential for cyclic AMP-dependent UCP1 expression in adipocytes. Mol Cell Biol 25: 5466–5479.

77. ThorntonTM, RinconM (2009) Non-classical p38 map kinase functions: cell cycle checkpoints and survival. International journal of biological sciences 5: 44–51.

78. BulavinDV, PhillipsC, NannengaB, TimofeevO, DonehowerLA, et al. (2004) Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nature genetics 36: 343–350.

79. Aguirre-GhisoJA (2007) Models, mechanisms and clinical evidence for cancer dormancy. Nature reviews Cancer 7: 834–846.

80. CarobbioS, RosenB, Vidal-PuigA (2013) Adipogenesis-New insights into brown adipose tissue differentiation. J MolEndocrinol 26: T75–85 doi: 10.1530/JME-13-0158

81. NedergaardJ, BengtssonT, CannonB (2007) Unexpected evidence for active brown adipose tissue in adult humans. American journal of physiology Endocrinology and metabolism 293: E444–452.

82. BeauvaisDM, BurbachBJ, RapraegerAC (2004) The syndecan-1 ectodomain regulates alphavbeta3 integrin activity in human mammary carcinoma cells. The Journal of cell biology 167: 171–181.

83. GaoY, NelsonDW, BanhT, YenMI, YenCL (2013) Intestine-specific expression of MOGAT2 partially restores metabolic efficiency in Mogat2-deficient mice. Journal of lipid research 54: 1644–1652.

84. PassonneauJV, LauderdaleVR (1974) A comparison of three methods of glycogen measurement in tissues. Analytical biochemistry 60: 405–412.