Glucocorticoid receptor mediates the expansion of splenic late erythroid progenitors during chronic psychological stress

Journal of Physiology and Pharmacology

Volumn 66, Issue 1, 2015, Pages 91-100

  Vignjevic, S ^a   Budec, Mirela ^a   Markovic, D ^a   Dikic, D ^a   Mitrovic, O ^a   Diklic, M ^a   Suboticki, T ^a   Cokic, V ^a   Jovcic, G ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Corticosterone; Erythroid progenitors; Glucocorticoid receptor; Psychological stress; Spleen

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; MIFEPRISTONE; BIOLOGICAL MARKER; CORTISONE; HORMONE ANTAGONIST;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CFU COUNTING; CONTROLLED STUDY; ERYTHROID CELL; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; HOMEOSTASIS; IMMUNE SYSTEM; IMMUNOHISTOCHEMISTRY; MALE; MENTAL STRESS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RADIOIMMUNOASSAY; SPLEEN WEIGHT; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; CBA MOUSE; CELL CULTURE; CELL PROLIFERATION; CHRONIC DISEASE; DISEASE MODEL; DRUG EFFECTS; ETIOLOGY; EXERCISE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; SPLEEN; TIME;

ANIMALS; BIOMARKERS; CELL PROLIFERATION; CELLS, CULTURED; CHRONIC DISEASE; CORTISONE; DISEASE MODELS, ANIMAL; ERYTHROID PRECURSOR CELLS; ERYTHROPOIESIS; HORMONE ANTAGONISTS; MALE; MICE, INBRED CBA; RECEPTORS, GLUCOCORTICOID; RESTRAINT, PHYSICAL; SIGNAL TRANSDUCTION; SPLEEN; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 84923183085     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Carrasco GA, Van de Kar LD. Neuroendocrine pharmacology of stress. Eur J Pharmacol 2003; 463: 235-272.
2. Joels M, Baram TZ. The neuro-symphony of stress. Nat Rev Neurosci 2009; 10: 459-466.
3. Patchev VK, Patchev AV. Experimental models of stress. Dialogues Clin Neurosci 2006; 8: 417-432.
4. Buynitsky T, Mostofsky DI. Restraint stress in biobehavioral research: recent developments. Neurosci Biobehav Rev 2009; 33: 1089-1098.
5. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 2000; 21: 55-89.
6. Riedemann T, Patchev AV, Cho K, Almeida OF. Corticosteroids: way upstream. Mol Brain 2010; 3: 2.
7. Chen W, Dang T, Blind RD, et al. Glucocorticoid receptor phosphorylation differentially affects target gene expression. Mol Endocrinol 2008; 22: 1754-1766.
8. Gursoy A, Dogruk Unal A, Ayturk S, et al. Polycythemia as the first manifestation of Cushing’s disease. J Endocrinol Invest 2006; 29: 742-744.
9. Hattangadi SM, Wong P, Zhang L, Flygare J, Lodish HF. From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood 2011; 118: 6258-6268.
10. Socolovsky M. Molecular insights into stress erythropoiesis. Curr Opin Hematol 2007; 14: 215-224.
11. Bauer A, Tronche F, Wessely O, et al. The glucocorticoid receptor is required for stress erythropoiesis. Genes Dev 1999; 13: 2996-3002.
12. Lodish H, Flygare J, Chou S. From stem cell to erythroblast: regulation of red cell production at multiple levels by multiple hormones. IUBMB Life 2010; 62: 492-496.
13. Paulson RF, Shi L, Wu DC. Stress erythropoiesis: new signals and new stress progenitor cells. Curr Opin Hematol 2011; 18: 139-145.
14. Perry JM, Harandi OF, Paulson RF. BMP4, SCF and hypoxia cooperatively regulate the expansion of murine stress erythroid progenitors. Blood 2007; 109: 4494-4502.
15. Perry JM, Harandi OF, Porayette P, Hegde S, Kannan AK, Paulson RF. Maintenance of the BMP4-dependent stress erythropoiesis pathway in the murine spleen requires hedgehog signaling. Blood 2009; 113: 911-918.
16. O’Neill HC. Niches for extramedullary hematopoiesis in the spleen. Niche 2012; 1: 12-16.
17. Lenox LE, Perry JM, Paulson RF. BMP4 and Madh5 regulate the erythroid response to acute anemia. Blood 2005; 105: 2741-2748.
18. Dumitriu B, Bhattaram P, Dy P, et al. Sox6 is necessary for efficient erythropoiesis in adult mice under physiological and anemia-induced stress conditions. PLoS One 2010; 5: e12088.
19. Ottenweller JE, Servatius RJ, Natelson BH. Repeated stress persistently elevates morning, but not evening, plasma corticosterone levels in male rats. Physiol Behav 1994; 55: 337-340.
20. Branch DR, Calderwood S, Cecutti MA, Herst R, Solh H. Hematopoietic progenitor cells are resistant to dimethyl sulfoxide toxicity. Transfusion 1994; 34: 887-890.
21. Kleinschnitz C, Blecharz K, Kahles T, et al. Glucocorticoid insensitivity at the hypoxic blood-brain barrier can be reversed by inhibition of the proteasome. Stroke 2011; 42: 1081-1089.
22. Budec M, Vignjevic S, Markovic D, et al. Effects of chronic psychological stress on extramedullary erythropoiesis: involvement of EPOR, GR, c-kit and BMP4 signaling. Haematologica 2013; 98(s1): 418.
23. Yarushkina NI, Bagaeva TR, Filaretova LP. Central corticotropin-releasing factor (CRF) may attenuate somatic pain sensitivity through involvement of glucocorticoids. J Physiol Pharmacol 2011; 62: 541-548.
24. Tsiftsoglou AS, Vizirianakis IS, Strouboulis J. Erythropoiesis: model systems, molecular regulators, and developmental programs. IUBMB Life 2009; 61: 800-830.
25. Hara H, Ogawa M. Erythropoietic precursors in mice with phenylhydrazine-induced anemia. Am J Hematol 1976, 1: 453-458.
26. Dor FJ, Ramirez ML, Parmar K, et al. Primitive hematopoietic cell populations reside in the spleen: studies in the pig, baboon, and human. Exp Hematol 2006; 34: 1573-1582.
27. Morita Y, Iseki A, Okamura S, Suzuki S, Nakauchi H, Ema H. Functional characterization of he matopoietic stem cells in the spleen. Exp Hematol 2011; 39: 351-359.
28. Yanai N, Matsuya Y, Obinata M. Spleen stromal cell lines selectively support erythroid colony formation. Blood 1989; 74: 2391-2397.
29. Vignjevic S, Budec M, Markovic D, et al. Chronic psychological stress activates BMP4-dependent extramedullary erythropoiesis. J Cell Mol Med 2014; 18: 91-103.
30. Engler H, Bailey MT, Engler A, Sheridan JF. Effects of repeated social stress on leukocyte distribution in bone marrow, peripheral blood and spleen. J Neuroimmunol 2004; 148: 106-115.
31. Stiner-Jones L, Reader B, Minnillo J, Sheridan J. Restraint stress alters innate immunity. Brain Behav Immun 2012; 26 (s1): S41-S42.
32. Bowers SL, Bilbo SD, Dhabhar FS, Nelson RJ. Stressorspecific alterations in corticosterone and immune responses inmice. Brain Behav Immun 2008; 22: 105-113.
33. Hernandez ME, Martinez-Mota L, Salinas C, et al. Chronic stress induces structural alterations in splenic lymphoid tissue that are associated with changes in corticosterone levels in Wistar-Kyoto rats. Biomed Res Int 2013; 2013: 868742.
34. Bakovic D, Pivac N, Zubin Maslov P, Breskovic T, Damonja G, Dujic Z. Spleen volume changes during adrenergic stimulation with low doses of epinephrine. J Physiol Pharmacol 2013; 64: 649-655.
35. Kerenyi MA, Orkin SH. Networking erythropoiesis. J Exp Med 2010; 207: 2537-2541.
36. Vanhees K, Coort S, Ruijters EJ, et al. Epigenetics: prenatal exposure to genistein leaves a permanent signature on the hematopoietic lineage. FASEB J 2011; 25: 797-807.
37. Kaminska B, Ciereszko R, Kiezun M, Dusza L. In vitro effects of genistein and daidzein on the activity of adrenocortical steroidogenic enzymes in mature female pigs. J Physiol Pharmacol 2013; 64: 103-108.
38. Voorhees JL, Powell ND, Moldovan L, Mo X, Eubank TD, Marsh CB. Chronic restraint stress upregulates erythropoiesis through glucocorticoid stimulation. PloS One 2013; 8: e77935.
39. McEwen BS. The neurobiology of stress: from serendipity to clinical relevance. Brain Res 2000; 886: 172-189.
40. Udupa KB, Crabtree HM, Lipschitz DA. In vitroculture of proerythroblasts: characterization of proliferative response to erythropoietin and steroids. Br J Haematol 1986; 62: 705-714.
41. Liang R, Chan TK, Todd D. Childhood acute lymphoblastic leukaemia and aplastic anaemia. Leuk Lymphoma 1994; 13: 411-415.
42. Necela BM, Cidlowski JA. Mechanisms of glucocorticoid receptor action in noninflammatory and inflammatory cells. Proc Am Thorac Soc 2004; 1: 239-246.
43. von Lindern M, Zauner W, Mellitzer G, et al. The glucocorticoid receptor cooperates with the erythropoietin receptor and c-Kit to enhance and sustain proliferation of erythroid progenitors in vitro. Blood 1999; 94: 550-559.
44. Chute JP, Ross JR, McDonnell DP. Minireview: Nuclear receptors, hematopoiesis, and stem cells. Mol Endocrinol 2010; 24: 1-10.
45. Wessely O, Deiner EM, Beug H, von Lindern M. The glucocorticoid receptor is a key regulator of the decision between self-renewal and differentiation in erythroid progenitors. EMBO J 1997; 16: 267-280.
46. Kolbus A, Blazquez-Domingo M, Carotta S et al. Cooperative signaling between cytokine receptorsand the glucocorticoid receptorin the expansion of erythroid progenitors: molecular analysis by expression profiling. Blood 2003; 102: 3136-3146.
47. Zhang L, Prak L, Rayon-Estrada V, et al. ZFP36L2 is required for self-renewal of early burst-forming unit erythroid progenitors. Nature 2013; 499: 92-96.
48. Flygare J, Rayon Estrada V, Shin C, Gupta S, Lodish HF. HIF1alpha synergizes with glucocorticoids to promote BFUE progenitor self-renewal. Blood 2011; 117: 3435-3444.
49. Millot S, Andrieu V, Letteron P, et al. Erythropoietin stimulates spleen BMP4-dependent stress erythropoiesis and partially corrects anemia in a mouse model of generalized inflammation. Blood 2010; 116: 6072-6081.
50. Richmond TD, Chohan M, Barber DL. Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol 2005; 15: 146-155.
51. Engler H, Bailey MT, Engler A, Stiner-Jones LM, Quan N, Sheridan JF. Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 2008; 33: 108-117.
52. Cohen S, Janicki-Deverts D, Doyle WJ, et al. Chronic stress, glucocorticoid receptorresistance, inflammation, anddiseaserisk. Proc Natl Acad Sci USA 2012; 109: 5995-5999.
53. Stellacci E, Di Noia A, Di Baldassarre A, Migliaccio G, Battistini A, Migliaccio AR. Interaction between the glucocorticoid and erythropoietin receptors in human erythroid cells. Exp Hematol 2009; 37: 559-572.
54. Varricchio L, Masselli E, Alfani E, et al. The dominant negative b isoform of the glucocorticoid receptor is uniquely expressed in erythroid cells expanded from polycythemia vera patients. Blood 2011; 118: 425-436.