Hepatic Hedgehog signaling contributes to the regulation of IGF1 and IGFBP1 serum levels

Cell Communication and Signaling

Volumn 12, Issue 1, 2014, Pages

  Matz Soja, Madlen ^a   Aleithe, Susanne ^a   Marbach, Eugenia ^a   Böttger, Jan ^a   Arnold, Katrin ^a   Schmidt Heck, Wolfgang ^b   Kratzsch, Jürgen ^a   Gebhardt, Rolf ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b HANS KNÖLL INSTITUTE   (Germany)

Author keywords

Gli3; Growth hormone; Hedgehog signaling; Hepatocytes; IGF I; IGFBP 1; Liver; MotifMap; Patched1; Smoothened

Indexed keywords

AMINOTRANSFERASE; GROWTH HORMONE; LIVER PROTEIN; MESSENGER RNA; PROTEIN PATCHED 1; RECEPTOR PROTEIN; SMALL INTERFERING RNA; SOMATOMEDIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI3; CELL SURFACE RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLI3 PROTEIN, MOUSE; IHH PROTEIN, MOUSE; INSULIN LIKE GROWTH FACTOR 1, MOUSE; INSULIN-LIKE GROWTH FACTOR-1, MOUSE; KRUPPEL LIKE FACTOR; NERVE PROTEIN; PATCHED RECEPTORS; SMO PROTEIN, MOUSE; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN C;

AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL COMPOSITION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE DELETION; GENE EXPRESSION; GENE REPRESSION; GROWTH HORMONE BLOOD LEVEL; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; LIVER CELL; LIVER SIZE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; UPREGULATION; WEIGHT GAIN; ANIMAL; BLOOD; CELL CULTURE; CYTOLOGY; GENETICS; HOMEOSTASIS; LIVER; METABOLISM; SIGNAL TRANSDUCTION; VASCULARIZATION;

ANIMALS; CELLS, CULTURED; FEMALE; HEDGEHOG PROTEINS; HEPATOCYTES; HOMEOSTASIS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 1; INSULIN-LIKE GROWTH FACTOR I; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIVER; MALE; MICE; NERVE TISSUE PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84896138369     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-12-11     Document Type: Article

References (53)

1. Learning from Jekyll to control Hyde: Hedgehog signaling in development and cancer. Barakat MT, Humke EW, Scott MP, Trends in Molecular Medicine 2010 16 337 348 10.1016/j.molmed.2010.05.003 20696410
2. Mechanisms and functions of Hedgehog signalling across the metazoa. Ingham PW, Nakano Y, Seger C, Nat Rev Genet 2011 12 393 406 10.1038/nrg2984 21502959
3. Evaluating Smoothened as a G-protein-coupled receptor for Hedgehog signalling. Ayers KL, Therond PP, Trends Cell Biol 2010 20 287 298 10.1016/j.tcb.2010.02.002 20207148
4. Mechanism and evolution of cytosolic Hedgehog signal transduction. Wilson CW, Chuang PT, Development 2010 137 2079 2094 10.1242/dev.045021 20530542
5. Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Ruiz I, Altaba A, Development 1999 126 3205 3216 10375510 (Pubitemid 29378183)
6. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Sasaki H, Nishizaki Y, Hui C, Nakafuku M, Kondoh H, Development 1999 126 3915 3924 10433919 (Pubitemid 29440488)
7. Hedgehog signaling in cancer formation and maintenance. Di Pasca MM, Hebrok M, Nat Rev Cancer 2003 3 903 911 10.1038/nrc1229 14737121 (Pubitemid 37500175)
8. Gli proteins and Hedgehog signaling: development and cancer. Ruiz I, Altaba A, Trends Genet 1999 15 418 425 10.1016/S0168-9525(99)01840-5 10498938 (Pubitemid 29469073)
9. Hedgehog signaling in development and homeostasis of the gastrointestinal tract. van den Brink GR, Physiol Rev 2007 87 1343 1375 10.1152/physrev.00054. 2006 17928586 (Pubitemid 350033824)
10. Disruption of hedgehog signaling reveals a novel role in intestinal morphogenesis and intestinal-specific lipid metabolism in mice. Wang LC, Nassir F, Liu ZY, Ling L, Luo F, Crowell T, Olson D, Davidson NO, Burkly LC, Gastroenterology 2002 122 469 482 10.1053/gast.2002.31102 11832461 (Pubitemid 34116998)
11. Hedgehog partial agonism drives Warburg-like metabolism in muscle and brown fat. Teperino R, Amann S, Bayer M, McGee SL, Loipetzberger A, Connor T, Jaeger C, Kammerer B, Winter L, Wiche G, Dalgaard K, Selvaraj M, Gaster M, Lee-Young RS, Febbraio MA, Knauf C, Cani PD, Aberger F, Penninger JM, Pospisilik JA, Esterbauer H, Cell 2012 151 414 426 10.1016/j.cell.2012.09.021 23063129
12. Drosophila genome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Pospisilik JA, Schramek D, Schnidar H, Cronin SJF, Nehme NT, Zhang X, Knauf C, Cani PD, Aumayr K, Todoric J, Bayer M, Haschemi A, Puviindran V, Tar K, Orthofer M, Neely GG, Dietzl G, Manoukian A, Funovics M, Prager G, Wagner O, Ferrandon D, Aberger F, Hui C, Esterbauer H, Penninger JM, Cell 2010 140 148 160 10.1016/j.cell.2009.12.027 20074523
13. Role for hedgehog signaling in hepatic stellate cell activation and viability. Sicklick JK, Li Y, Choi SS, Qi Y, Chen W, Bustamante M, Huang J, Zdanowicz M, Camp T, Torbenson MS, Rojkind M, Diehl AM, Lab Invest 2005 85 1368 1380 10.1038/labinvest.3700349 16170335 (Pubitemid 41509385)
14. Hedgehog signaling in cholangiocytes. Omenetti A, Diehl AM, Curr Opin Gastroenterol 2011 27 268 275 10.1097/MOG.0b013e32834550b4 21423008
15. Signals from dying hepatocytes trigger growth of liver progenitors. Jung Y, Witek RP, Syn WK, Choi SS, Omenetti A, Premont R, Guy CD, Diehl AM, Gut 2010 59 655 665 10.1136/gut.2009.204354 20427400
16. Increased production of sonic hedgehog by ballooned hepatocytes. Rangwala F, Guy CD, Lu J, Suzuki A, Burchette JL, Abdelmalek MF, Chen W, Diehl AM, J. Pathol 2011 224 401 410 10.1002/path.2888 21547909
17. Hedgehog signaling in the liver. Omenetti A, Choi S, Michelotti G, Diehl AM, J Hepatol 2011 54 366 373 21093090
18. Hedgehog signaling pathway in adult liver: a major new player in hepatocyte metabolism and zonation? Matz-Soja M, Hovhannisyan A, Gebhardt R, Med Hypotheses 2013 80 589 594 10.1016/j.mehy.2013.01.032 23433827
19. Patched acts catalytically to suppress the activity of Smoothened. Taipale J, Cooper MK, Maiti T, Beachy PA, Nature 2002 418 892 897 10.1038/nature00989 12192414 (Pubitemid 34966310)
20. Hepatocyte-specific expression of Cre recombinase. Kellendonk C, Opherk C, Anlag K, Schutz G, Tronche F, Genesis 2000 26 151 153 10.1002/(SICI)1526- 968X(200002)26:2<151::AID-GENE17>3.0.CO;2-E 10686615 (Pubitemid 30158105)
21. Disruption of the growth hormone-Signal transducer and activator of transcription 5-Insulinlike growth factor 1 axis severely aggravates liver fibrosis in a mouse model of cholestasis. Blaas L, Kornfeld J, Schramek D, Musteanu M, Zollner G, Gumhold J, van Zijl F, Schneller D, Esterbauer H, Egger G, Mair M, Kenner L, Mikulits W, Eferl R, Moriggl R, Penninger J, Trauner M, Casanova E, Hepatology 2010 51 1319 1326 10.1002/hep.23469 20162728
22. Response of sinusoidal mouse liver cells to choline-deficient ethionine-supplemented diet. Ueberham E, Bottger J, Ueberham U, Grosche J, Gebhardt R, Comp Hepatol 2010 9 8 10.1186/1476-5926-9-8 20942944
23. Glutamate uptake in primary cultures of biliary epithelial cells from normal rat liver. Eisenmann-Tappe I, Wizigmann S, Gebhardt R, Cell Biol Toxicol 1991 7 315 325 10.1007/BF00124068 1724409
24. Identification of Hedgehog pathway components by RNAi in Drosophila cultured cells. Lum L, Yao S, Mozer B, Rovescalli A, Von KD, Nirenberg M, Beachy PA, Science 2003 299 2039 2045 10.1126/science.1081403 12663920 (Pubitemid 36383726)
25. Possible roles of insulin-like growth factor in regulation of physiological and pathophysiological liver growth. Skrtic S, Wallenius K, Sjogren K, Isaksson OG, Ohlsson C, Jansson JO, Horm Res 2001 55 Suppl 1 1 6
26. Altered neural cell fates and medulloblastoma in mouse patched mutants. Goodrich LV, Milenkovic L, Higgins KM, Scott MP, Science 1997 277 1109 1113 10.1126/science.277.5329.1109 9262482 (Pubitemid 27371635)
27. MotifMap: integrative genome-wide maps of regulatory motif sites for model species. Daily K, Patel VR, Rigor P, Xie X, Baldi P, BMC Bioinformatics 2011 12 495 10.1186/1471-2105-12-495 22208852
28. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Udy GB, Towers RP, Snell RG, Wilkins RJ, Park SH, Ram PA, Waxman DJ, Davey HW, Proc Natl Acad Sci USA 1997 94 7239 7244 10.1073/pnas.94.14.7239 9207075 (Pubitemid 27345299)
29. Dispersed Chromosomal Stat5b-binding elements mediate growth hormone-activated insulin-like growth factor-I gene transcription. Chia DJ, Varco-Merth B, Rotwein P, J Biol Chem 2010 285 17636 17647 10.1074/jbc.M110. 117697 20378540
30. Hedgehog signaling maintains resident hepatic progenitors throughout life. Sicklick JK, Li Y, Melhem A, Schmelzer E, Zdanowicz M, Huang J, Caballero M, Fair JH, Ludlow JW, McClelland RE, Reid LM, Diehl AM, Am J Physiol Gastrointest Liver Physiol 2006 290 859 70 16322088
31. Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. Dai P, Akimaru H, Tanaka Y, Maekawa T, Nakafuku M, Ishii S, J Biol Chem 1999 274 8143 8152 10.1074/jbc.274.12.8143 10075717 (Pubitemid 29144290)
32. Metabolic zonation of the liver: regulation and implications for liver function. Gebhardt R, Pharmacol Ther 1992 53 275 354 10.1016/0163-7258(92)90055- 5 1409850
33. Organ patterning in the adult stage: the role of Wnt/beta-catenin signaling in liver zonation and beyond. Gebhardt R, Hovhannisyan A, Dev Dyn 2010 239 45 55 19705440
34. B-catenin deficiency, but not Myc deletion, suppresses the immediate phenotypes of APC loss in the liver. Reed KR, Athineos D, Meniel VS, Wilkins JA, Ridgway RA, Burke ZD, Muncan V, Clarke AR, Sansom OJ, Proc Natl Acad Sci USA. 2008 105 18919 23 10.1073/pnas.0805778105 19033191
35. Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Sjogren K, Liu JL, Blad K, Skrtic S, Vidal O, Wallenius V, LeRoith D, Tornell J, Isaksson OG, Jansson JO, Ohlsson C, Proc Natl Acad Sci USA 1999 96 7088 7092 10.1073/pnas.96.12.7088 10359843 (Pubitemid 29275014)
36. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Vokes SA, Ji H, Wong WH, McMahon AP, Genes Dev 2008 22 2651 2663 10.1101/gad.1693008 18832070
37. Liver-specific expression of human insulin-like growth factor binding protein-1 in transgenic mice: repercussions on reproduction, ante- and perinatal mortality and postnatal growth. Gay E, Seurin D, Babajko S, Doublier S, Cazillis M, Binoux M, Endocrinology 1997 138 2937 2947 9202238 (Pubitemid 27258527)
38. Transgenic mouse models for studying the functions of insulin-like growth factor-binding proteins. Schneider MR, Lahm H, Wu M, Hoeflich A, Wolf E, FASEB J 2000 14 629 640 10744620 (Pubitemid 30198562)
39. Regulation and function of insulin-like growth factor-binding protein-1. Lee PD, Conover CA, Powell DR, Proc Soc Exp Biol Med 1993 204 4 29 10.3181/00379727-204-43630 7690486 (Pubitemid 23274051)
40. Assessment of growth hormone status in acromegaly: what biochemical markers to measure and how? Camacho-Hubner C, Growth Horm IGF Res 2000 10 125 9 10984268
41. Liver-derived IGF-I is of importance for normal carbohydrate and lipid metabolism. Sjogren K, Wallenius K, Liu JL, Bohlooly-Y M, Pacini G, Svensson L, Tornell J, Isaksson OG, Ahren B, Jansson JO, Ohlsson C, Diabetes 2001 50 1539 1545 10.2337/diabetes.50.7.1539 11423474 (Pubitemid 33639593)
42. Normal growth and development in the absence of hepatic insulin-like growth factor I. Yakar S, Liu JL, Stannard B, Butler A, Accili D, Sauer B, LeRoith D, Proc Natl Acad Sci USA 1999 96 7324 7329 10.1073/pnas.96.13.7324 10377413 (Pubitemid 29299660)
43. Overexpression of insulin-like growth factor binding protein-1 in transgenic mice. Murphy LJ, Pediatr Nephrol 2000 14 567 571 10.1007/ s004670000347 10912520 (Pubitemid 30394430)
44. Role of insulin-like growth factor in maintaining normal glucose homeostasis. Clemmons DR, Horm Res 2004 62 Suppl 1 77 82 15761237 (Pubitemid 40529154)
45. Insulin-like growth factor binding protein: a possible marker for the metabolic syndrome? Ruan W, Lai M, Acta Diabetol 2010 47 5 14 10.1007/s00592-009-0142-3 19771387
46. Reproductive abnormalities in human IGF binding protein-1 transgenic female mice. Froment P, Seurin D, Hembert S, Levine JE, Pisselet C, Monniaux D, Binoux M, Monget P, Endocrinology 2002 143 1801 1808 10.1210/endo.143.5.8815 11956162 (Pubitemid 34415895)
47. Genetic coregulation of age of female sexual maturation and lifespan through circulating IGF1 among inbred mouse strains. Yuan R, Meng Q, Nautiyal J, Flurkey K, Tsaih S, Krier R, Parker MG, Harrison DE, Paigen B, Proc Natl Acad Sci USA 2012 109 8224 8229 10.1073/pnas.1121113109 22566614
48. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Long F, Zhang XM, Karp S, Yang Y, McMahon AP, Development 2001 128 5099 5108 11748145 (Pubitemid 34086893)
49. Stringent doxycycline dependent control of CRE recombinase in vivo. Schonig K, Schwenk F, Rajewsky K, Bujard H, Nucleic Acids Res 2002 30 134 10.1093/nar/gnf134 12466566
50. 4-Aminoethylamino-emodin-a novel potent inhibitor of GSK-3beta-acts as an insulin-sensitizer avoiding downstream effects of activated beta-catenin. Gebhardt R, Lerche KS, Gotschel F, Gunther R, Kolander J, Teich L, Zellmer S, Hofmann H, Eger K, Hecht A, Gaunitz F, J Cell Mol Med 2010 14 1276 1293 10.1111/j.1582-4934.2009.00701.x 19228266
51. Primary mouse hepatocytes for systems biology approaches: a standardized in vitro system for modelling of signal transduction pathways. Klingmuller U, Bauer A, Bohl S, Nickel PJ, Breitkopf K, Dooley S, Zellmer S, Kern C, Merfort I, Sparna T, Donauer J, Walz G, Geyer M, Kreutz C, Hermes M, Gotschel F, Hecht A, Walter D, Egger L, Neubert K, Borner C, Brulport M, Schormann W, Sauer C, Baumann F, Preiss R, MacNelly S, Godoy P, Wiercinska E, Ciuclan L, et al. Syst Biol (Stevenage) 2006 153 433 447 10.1049/ip-syb:20050067 17186705 (Pubitemid 44712259)
52. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL, BMC Bioinformatics. 2012 13 134 10.1186/1471-2105-13-134 22708584
53. Heterogeneous expression of suppressor of cytokine signaling 2 (SOCS-2) in liver tissue. Zellmer S, Sickinger S, Schmidt-Heck W, Guthke R, Gebhardt R, J Anat 2009 215 176 183 10.1111/j.1469-7580.2009.01085.x 19470084