Lipoproteins and Hedgehog signalling - possible implications for the adrenal gland function

European Journal of Clinical Investigation

Volumn 43, Issue 11, 2013, Pages 1178-1183

  Swierczynska, Marta M ^a,b   Lamounier Zepter, Valéria ^a   Bornstein, Stefan R ^a   Eaton, Suzanne ^b  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Adrenal gland; Lipoproteins; Metabolic syndrome; Sonic hedgehog

Indexed keywords

ANGIOTENSIN II; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; HYDROCORTISONE; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; SONIC HEDGEHOG PROTEIN; SHH PROTEIN, HUMAN;

ADRENAL CORTEX; ADRENAL FUNCTION; ADRENAL GLAND; HOMEOSTASIS; HYPOPLASIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STEROIDOGENESIS; VERTEBRATE; ADRENAL GLAND DISEASES; ADULT; HUMAN; METABOLIC SYNDROME X; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADRENAL GLAND DISEASES; ADRENAL GLANDS; ADULT; HEDGEHOG PROTEINS; HUMANS; LIPOPROTEINS; METABOLIC SYNDROME X; SIGNAL TRANSDUCTION;

EID: 84885419722     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/eci.12145     Document Type: Review

References (58)

1. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet 2005;365:1415-28.
2. Krug AW, Ehrhart-Bornstein M. Adrenocortical dysfunction in obesity and the metabolic syndrome. Horm Metab Res 2008;40:515-7.
3. Sowers JR, Whaley-Connell A, Epstein M. Narrative review: the emerging clinical implications of the role of aldosterone in the metabolic syndrome and resistant hypertension. Ann Intern Med 2009;150:776-83.
4. Whaley-Connell A, Johnson MS, Sowers JR. Aldosterone: role in the cardiometabolic syndrome and resistant hypertension. Prog Cardiovasc Dis 2010;52:401-9.
5. Roberge C, Carpentier AC, Langlois MF, Baillargeon JP, Ardilouze JL, Maheux P et al. Adrenocortical dysregulation as a major player in insulin resistance and onset of obesity. Am J Physiol Endocrinol Metab 2007;293:E1465-78.
6. Wang M. The role of glucocorticoid action in the pathophysiology of the Metabolic Syndrome. Nutr Metab (Lond) 2005;2:3.
7. Pasquali R, Vicennati V. Activity of the hypothalamic-pituitary-adrenal axis in different obesity phenotypes. Int J Obes Relat Metab Disord 2000;24(Suppl 2):S47-9.
8. Thomson SP, Stump CS, Kurukulasuriya LR, Sowers JR. Adrenal steroids and the metabolic syndrome. Curr Hypertens Rep 2007;9:512-9.
9. Bornstein SR, Engeland WC, Ehrhart-Bornstein M, Herman JP. Dissociation of ACTH and glucocorticoids. Trends Endocrinol Metab 2008;19:175-80.
10. Walker BR. Cortisol-cause and cure for metabolic syndrome? Diabet Med 2006;23:1281-8.
11. Briet M, Schiffrin EL. The role of aldosterone in the metabolic syndrome. Curr Hypertens Rep 2011;13:163-72.
12. Fujita T. Mineralocorticoid receptors, salt-sensitive hypertension, and metabolic syndrome. Hypertension 2010;55:813-8.
13. Kraemer FB. Adrenal cholesterol utilization. Mol Cell Endocrinol 2007;265-266:42-5.
14. Gwynne JT, Strauss JF 3rd. The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands. Endocr Rev 1982;3:299-329.
15. Martin G, Pilon A, Albert C, Valle M, Hum DW, Fruchart JC et al. Comparison of expression and regulation of the high-density lipoprotein receptor SR-BI and the low-density lipoprotein receptor in human adrenocortical carcinoma NCI-H295 cells. Eur J Biochem 1999;261:481-91.
16. Illingworth DR, Lees AM, Lees RS. Adrenal cortical function in homozygous familial hypercholesterolemia. Metabolism 1983;32:1045-52.
17. Vergeer M, Korporaal SJ, Franssen R, Meurs I, Out R, Hovingh GK et al. Genetic variant of the scavenger receptor BI in humans. N Engl J Med 2011;364:136-45.
18. Xing Y, Cohen A, Rothblat G, Sankaranarayanan S, Weibel G, Royer L et al. Aldosterone production in human adrenocortical cells is stimulated by high-density lipoprotein 2 (HDL2) through increased expression of aldosterone synthase (CYP11B2). Endocrinology 2011;152:751-63.
19. Saha S, Bornstein SR, Graessler J, Kopprasch S. Very-low-density lipoprotein mediates transcriptional regulation of aldosterone synthase in human adrenocortical cells through multiple signaling pathways. Cell Tissue Res 2012;348:71-80.
20. Xing Y, Rainey WE, Apolzan JW, Francone OL, Harris RB, Bollag WB. Adrenal cell aldosterone production is stimulated by very-low-density lipoprotein (VLDL). Endocrinology 2012;153:721-31.
21. Ansurudeen I, Pietzsch J, Graessler J, Ehrhart-Bornstein M, Saha S, Bornstein SR et al. Modulation of adrenal aldosterone release by oxidative modification of low-density lipoprotein. Am J Hypertens 2010;23:1061-8.
22. Kopprasch S, Pietzsch J, Ansurudeen I, Graessler J, Krug AW, Ehrhart-Bornstein M et al. Prediabetic and diabetic in vivo modification of circulating low-density lipoprotein attenuates its stimulatory effect on adrenal aldosterone and cortisol secretion. J Endocrinol 2009;200:45-52.
23. Berthon A, Martinez A, Bertherat J, Val P. Wnt/beta-catenin signalling in adrenal physiology and tumour development. Mol Cell Endocrinol 2012;351:87-95.
24. Ehrhart-Bornstein M, Hinson JP, Bornstein SR, Scherbaum WA, Vinson GP. Intraadrenal interactions in the regulation of adrenocortical steroidogenesis. Endocr Rev 1998;19:101-43.
25. Ehrhart-Bornstein M, Bornstein SR. Cross-talk between adrenal medulla and adrenal cortex in stress. Ann N Y Acad Sci 2008;1148:112-7.
26. Huang CC, Miyagawa S, Matsumaru D, Parker KL, Yao HH. Progenitor cell expansion and organ size of mouse adrenal is regulated by sonic hedgehog. Endocrinology 2010;151:1119-28.
27. King P, Paul A, Laufer E. Shh signaling regulates adrenocortical development and identifies progenitors of steroidogenic lineages. Proc Natl Acad Sci USA 2009;106:21185-90.
28. Ching S, Vilain E. Targeted disruption of Sonic Hedgehog in the mouse adrenal leads to adrenocortical hypoplasia. Genesis 2009;47:628-37.
29. Boulkroun S, Samson-Couterie B, Golib-Dzib JF, Amar L, Plouin PF, Sibony M et al. Aldosterone-producing adenoma formation in the adrenal cortex involves expression of stem/progenitor cell markers. Endocrinology 2011;152:4753-63.
30. Ingham PW, McMahon AP. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001;15:3059-87.
31. Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG et al. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 2003;39:937-50.
32. Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, Herzberg CD et al. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005;132:335-44.
33. Baron MH. Embryonic origins of mammalian hematopoiesis. Exp Hematol 2003;31:1160-9.
34. Ishizuya-Oka A, Hasebe T. Sonic hedgehog and bone morphogenetic protein-4 signaling pathway involved in epithelial cell renewal along the radial axis of the intestine. Digestion 2008;77(Suppl 1):42-7.
35. van den Brink GR. Hedgehog signaling in development and homeostasis of the gastrointestinal tract. Physiol Rev 2007;87:1343-75.
36. Adolphe C, Narang M, Ellis T, Wicking C, Kaur P, Wainwright B. An in vivo comparative study of sonic, desert and Indian hedgehog reveals that hedgehog pathway activity regulates epidermal stem cell homeostasis. Development 2004;131:5009-19.
37. Laufer E, Kesper D, Vortkamp A, King P. Sonic hedgehog signaling during adrenal development. Mol Cell Endocrinol 2012;351:19-27.
38. Levina E, Chen M, Carkner R, Shtutman M, Buttyan R. Paracrine Hedgehog increases the steroidogenic potential of prostate stromal cells in a Gli-dependent manner. Prostate 2012;72:817-24.
39. Spicer LJ, Sudo S, Aad PY, Wang LS, Chun SY, Ben-Shlomo I et al. The hedgehog-patched signaling pathway and function in the mammalian ovary: a novel role for hedgehog proteins in stimulating proliferation and steroidogenesis of theca cells. Reproduction 2009;138:329-39.
40. Mann RK, Beachy PA. Novel lipid modifications of secreted protein signals. Annu Rev Biochem 2004;73:891-923.
41. Palm W, Swierczynska MM, Kumari V, Ehrhart-Bornstein M, Bornstein SR, Eaton S. Secretion and signaling activities of lipoprotein-associated hedgehog and non-sterol-modified hedgehog in flies and mammals. PLoS Biol 2013;11:e1001505.
42. Panakova D, Sprong H, Marois E, Thiele C, Eaton S. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 2005;435:58-65.
43. Khaliullina H, Panakova D, Eugster C, Riedel F, Carvalho M, Eaton S. Patched regulates Smoothened trafficking using lipoprotein-derived lipids. Development 2009;136:4111-21.
44. Taipale J, Cooper MK, Maiti T, Beachy PA. Patched acts catalytically to suppress the activity of Smoothened. Nature 2002;418:892-7.
45. Hooper JE, Scott MP. Communicating with Hedgehogs. Nat Rev Mol Cell Biol 2005;6:306-17.
46. Lum L, Beachy PA. The Hedgehog response network: sensors, switches, and routers. Science 2004;304:1755-9.
47. Eaton S. Multiple roles for lipids in the Hedgehog signalling pathway. Nat Rev Mol Cell Biol 2008;9:437-45.
48. Chen JK, Taipale J, Young KE, Maiti T, Beachy PA. Small molecule modulation of Smoothened activity. Proc Natl Acad Sci USA 2002;99:14071-6.
49. Frank-Kamenetsky M, Zhang XM, Bottega S, Guicherit O, Wichterle H, Dudek H et al. Small-molecule modulators of Hedgehog signaling: identification and characterization of Smoothened agonists and antagonists. J Biol 2002;1:10.
50. Nachtergaele S, Mydock LK, Krishnan K, Rammohan J, Schlesinger PH, Covey DF et al. Oxysterols are allosteric activators of the oncoprotein Smoothened. Nat Chem Biol 2012;8:211-20.
51. Ioannou YA. Multidrug permeases and subcellular cholesterol transport. Nat Rev Mol Cell Biol 2001;2:657-68.
52. Ikonen E, Holtta-Vuori M. Cellular pathology of Niemann-Pick type C disease. Semin Cell Dev Biol 2004;15:445-54.
53. Mukherjee S, Maxfield FR. Lipid and cholesterol trafficking in NPC. Biochim Biophys Acta 2004;1685:28-37.
54. Infante RE, Radhakrishnan A, Abi-Mosleh L, Kinch LN, Wang ML, Grishin NV et al. Purified NPC1 protein: II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J Biol Chem 2008;283:1064-75.
55. Bassett JR, West SH. Vascularization of the adrenal cortex: its possible involvement in the regulation of steroid hormone release. Microsc Res Tech 1997;36:546-57.
56. Bishop JR, Stanford KI, Esko JD. Heparan sulfate proteoglycans and triglyceride-rich lipoprotein metabolism. Curr Opin Lipidol 2008;19:307-13.
57. Kolset SO, Salmivirta M. Cell surface heparan sulfate proteoglycans and lipoprotein metabolism. Cell Mol Life Sci 1999;56:857-70.
58. Zhang F, McLellan JS, Ayala AM, Leahy DJ, Linhardt RJ. Kinetic and structural studies on interactions between heparin or heparan sulfate and proteins of the hedgehog signaling pathway. Biochemistry 2007;46:3933-41.