全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

Chronic Restraint Stress Upregulates Erythropoiesis through Glucocorticoid Stimulation

DOI: 10.1371/journal.pone.0077935

Full-Text   Cite this paper   Add to My Lib

Abstract:

In response to elevated glucocorticoid levels, erythroid progenitors rapidly expand to produce large numbers of young erythrocytes. Previous work demonstrates hematopoietic changes in rodents exposed to various physical and psychological stressors, however, the effects of chronic psychological stress on erythropoiesis has not be delineated. We employed laboratory, clinical and genomic analyses of a murine model of chronic restraint stress (RST) to examine the influence of psychological stress on erythropoiesis. Mice exposed to RST demonstrated markers of early erythroid expansion involving the glucocorticoid receptor. In addition, these RST-exposed mice had increased numbers of circulating reticulocytes and increased erythropoiesis in primary and secondary erythroid tissues. Mice also showed increases in erythroid progenitor populations and elevated expression of the erythroid transcription factor KLF1 in these cells. Together this work reports some of the first evidence of psychological stress affecting erythroid homeostasis through glucocorticoid stimulation.

References

[1]  Gregory T, Yu C, Ma A, Orkin SH, Blobel GA et al. (1999) GATA-1 and erythropoietin cooperate to promote erythroid cell survival by regulating bcl-xL expression. Blood 94: 87-96. PubMed: 10381501.
[2]  Zhao W, Kitidis C, Fleming MD, Lodish HF, Ghaffari S (2006) Erythropoietin stimulates phosphorylation and activation of GATA-1 via the PI3-kinase/AKT signaling pathway. Blood 107: 907-915. PubMed: 16204311.
[3]  Hattangadi SM, Wong P, Zhang L, Flygare J, Lodish HF (2011) From stem cell to red cell: Regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood 118: 6258-6268. doi:10.1182/blood-2011-07-356006. PubMed: 21998215.
[4]  Dumitriu B, Bhattaram P, Dy P, Huang Y, Quayum N et al. (2010) Sox6 is necessary for efficient erythropoiesis in adult mice under physiological and anemia-induced stress conditions. PLOS ONE 5: e12088. doi:10.1371/journal.pone.0012088. PubMed: 20711497.
[5]  Lim GB, Dodic M, Earnest L, Jeyaseelan K, Wintour EM (1996) Regulation of erythropoietin gene expression in fetal sheep by glucocorticoids. Endocrinology 137: 1658-1663. doi:10.1210/en.137.5.1658. PubMed: 8612498.
[6]  Moritz KM, Lim GB, Wintour EM (1997) Developmental regulation of erythropoietin and erythropoiesis. Am J Physiol 273: R1829-R1844. PubMed: 9435635.
[7]  Fowden AL, Li J, Forhead AJ (1998) Glucocorticoids and the preparation for life after birth: Are there long-term consequences of the life insurance? Proc Nutr Soc 57: 113-122. doi:10.1079/PNS19980017. PubMed: 9571716.
[8]  Tang JI, Seckl JR, Nyirenda MJ (2011) Prenatal glucocorticoid overexposure causes permanent increases in renal erythropoietin expression and red blood cell mass in the rat offspring. Endocrinology 152: 2716-2721. doi:10.1210/en.2010-1443. PubMed: 21540288.
[9]  Golde DW, Bersch N, Cline MJ (1976) Potentiation of erythropoiesis in vitro by dexamethasone. J Clin Invest 57: 57-62. doi:10.1172/JCI108269. PubMed: 173742.
[10]  Anisman H, Kokkinidis L, Borowski T, Merali Z (1998) Differential effects of interleukin (IL)-1beta, IL-2 and IL-6 on responding for rewarding lateral hypothalamic stimulation. Brain Res 779: 177-187. doi:10.1016/S0006-8993(97)01114-1. PubMed: 9473665.
[11]  Udupa KB, Crabtree HM, Lipschitz DA (1986) In vitro culture of proerythroblasts: Characterization of proliferative response to erythropoietin and steroids. Br J Haematol 62: 705-714. doi:10.1111/j.1365-2141.1986.tb04094.x. PubMed: 3964563.
[12]  Bauer A, Tronche F, Wessely O, Kellendonk C, Reichardt HM et al. (1999) The glucocorticoid receptor is required for stress erythropoiesis. Genes Dev 13: 2996-3002. doi:10.1101/gad.13.22.2996. PubMed: 10580006.
[13]  Flygare J, Rayon Estrada V, Shin C, Gupta S, Lodish HF (2011) HIF1alpha synergizes with glucocorticoids to promote BFU-E progenitor self-renewal. Blood 117: 3435-3444. doi:10.1182/blood-2010-07-295550. PubMed: 21177435.
[14]  Patel S, Xi ZF, Seo EY, McGaughey D, Segre JA (2006) Klf4 and corticosteroids activate an overlapping set of transcriptional targets to accelerate in utero epidermal barrier acquisition. Proc Natl Acad Sci U S A 103: 18668-18673. doi:10.1073/pnas.0608658103. PubMed: 17130451.
[15]  Turner J, Crossley M (1998) Cloning and characterization of mCtBP2, a co-repressor that associates with basic kruppel-like factor and other mammalian transcriptional regulators. EMBO J 17: 5129-5140. doi:10.1093/emboj/17.17.5129. PubMed: 9724649.
[16]  Tallack MR, Whitington T, Yuen WS, Wainwright EN, Keys JR et al. (2010) A global role for KLF1 in erythropoiesis revealed by ChIP-seq in primary erythroid cells. Genome Res 20: 1052-1063. doi:10.1101/gr.106575.110. PubMed: 20508144.
[17]  Cantor AB, Orkin SH (2002) Transcriptional regulation of erythropoiesis: An affair involving multiple partners. Oncogene 21: 3368-3376. doi:10.1038/sj.onc.1205326. PubMed: 12032775.
[18]  Dygai AM, Skurikhin EG (2011) Monoaminergic regulation of hemopoiesis under extreme conditions. Bull Exp Biol Med 151: 171-178. doi:10.1007/s10517-011-1282-3. PubMed: 22238743.
[19]  de Souza Queiroz J, Malacrida SA, Justo GZ, Queiroz ML (2004) Myelopoietic response in mice exposed to acute cold/restraint stress: Modulation by chlorella vulgaris prophylactic treatment. Immunopharmacol Immunotoxicol 26: 455-467. doi:10.1081/IPH-200026914. PubMed: 15518178.
[20]  Malacrida SA, Teixeira NA, Queiroz ML (1997) Hematopoietic changes in rats after inescapable and escapable shocks. Immunopharmacol Immunotoxicol 19: 523-533. doi:10.3109/08923979709007673. PubMed: 9436051.
[21]  Malacrida SA, Teixeira NA, Queiroz ML (1997) Regulation of stress-induced reduced myelopoiesis in rats. Int J Immunopharmacol 19: 227-233. doi:10.1016/S0192-0561(97)00029-5. PubMed: 9373773.
[22]  Queiroz Jde S, Torello CO, Palermo-Neto J, Valadares MC, Queiroz ML (2008) Hematopoietic response of rats exposed to the impact of an acute psychophysiological stressor on responsiveness to an in vivo challenge with listeria monocytogenes: Modulation by chlorella vulgaris prophylactic treatment. Brain Behav Immun 22: 1056-1065. doi:10.1016/j.bbi.2008.03.002. PubMed: 18420376.
[23]  Méndez-Ferrer S, Lucas D, Battista M, Frenette PS (2008) Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452: 442-447. doi:10.1038/nature06685. PubMed: 18256599.
[24]  Kiank C, Holtfreter B, Starke A, Mundt A, Wilke C et al. (2006) Stress susceptibility predicts the severity of immune depression and the failure to combat bacterial infections in chronically stressed mice. Brain Behav Immun 20: 359-368. doi:10.1016/j.bbi.2005.10.151. PubMed: 16330179.
[25]  Bredel M, Bredel C, Juric D, Harsh GR, Vogel H et al. (2005) Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYC-interacting genes in human gliomas. Cancer Res 65: 8679-8689. doi:10.1158/0008-5472.CAN-05-1204. PubMed: 16204036.
[26]  Holm S (1979) A simple sequentially rejective multiple ATest procedure. Scand J Statist 6: 65-70.
[27]  Wohleb ES, Hanke ML, Corona AW, Powell ND, Stiner LM et al. (2011) Beta-adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J Neurosci 31: 6277-6288. doi:10.1523/JNEUROSCI.0450-11.2011. PubMed: 21525267.
[28]  Richmond TD, Chohan M, Barber DL (2005) Turning cells red: Signal transduction mediated by erythropoietin. Trends Cell Biol 15: 146-155. doi:10.1016/j.tcb.2005.01.007. PubMed: 15752978.
[29]  Borges L, Iacovino M, Mayerhofer T, Koyano-Nakagawa N, Baik J et al. (2012) A critical role for endoglin in the emergence of blood during embryonic development. Blood 119: 5417-5428. doi:10.1182/blood-2011-11-391896. PubMed: 22535663.
[30]  Sato S, Kozuma Y, Hasegawa Y, Kojima H, Chiba S et al. (2010) Enhanced expression of CD71, transferrin receptor, on immature reticulocytes in patients with paroxysmal nocturnal hemoglobinuria. Int J Lab Hematol 32: e137-e143. doi:10.1111/j.1751-553X.2009.01148.x. PubMed: 19302232.
[31]  Cao YA, Kusy S, Luong R, Wong RJ, Stevenson DK et al. (2011) Heme oxygenase-1 deletion affects stress erythropoiesis. PLOS ONE 6: e20634. doi:10.1371/journal.pone.0020634. PubMed: 21655188.
[32]  Voorhees JL, Tarr AJ, Wohleb ES, Godbout JP, Mo X et al. (2013) Prolonged restraint stress increases IL-6, reduces IL-10, and causes persistent depressive-like behavior that is reversed by recombinant IL-10. PLOS ONE 8: e58488. doi:10.1371/journal.pone.0058488. PubMed: 23520517.
[33]  Tiedt R, Hao-Shen H, Sobas MA, Looser R, Dirnhofer S et al. (2008) Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice. Blood 111: 3931-3940. doi:10.1182/blood-2007-08-107748. PubMed: 18160670.
[34]  Tripathy SK, Svensson EC, Black HB, Goldwasser E, Margalith M et al. (1996) Long-term expression of erythropoietin in the systemic circulation of mice after intramuscular injection of a plasmid DNA vector. Proc Natl Acad Sci U S A 93: 10876-10880. doi:10.1073/pnas.93.20.10876. PubMed: 8855275.
[35]  Boyle MP, Brewer JA, Funatsu M, Wozniak DF, Tsien JZ et al. (2005) Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc Natl Acad Sci U S A 102: 473-478. doi:10.1073/pnas.0406458102. PubMed: 15623560.
[36]  Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: When the immune system subjugates the brain. Nat Rev Neurosci 9: 46-56. doi:10.1038/nrn2297. PubMed: 18073775.
[37]  Maccari S, Morley-Fletcher S (2007) Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32 Suppl 1: S10-S15. doi:10.1016/j.psyneuen.2007.06.005. PubMed: 17651905.
[38]  Solomon MB, Furay AR, Jones K, Packard AE, Packard BA et al. (2011) Deletion of forebrain glucocorticoid receptors impairs neuroendocrine stress responses and induces depression-like behavior in males but not females. Neuroscience .
[39]  Maes M, Van de Vyvere J, Vandoolaeghe E, Bril T, Demedts P et al. (1996) Alterations in iron metabolism and the erythron in major depression: Further evidence for a chronic inflammatory process. J Affect Disord 40: 23-33. doi:10.1016/0165-0327(96)00038-9. PubMed: 8882911.
[40]  van West D, Maes M (1999) Activation of the inflammatory response system: A new look at the etiopathogenesis of major depression. Neuro Endocrinol Lett 20: 11-17. PubMed: 11473226.
[41]  Turney TH, Harmsen AG (1984) Splenomegaly and other hematological parameters in the socially dominant mouse. Physiol Behav 33: 559-562. doi:10.1016/0031-9384(84)90371-8. PubMed: 6543009.
[42]  Allen DL, McCall GE, Loh AS, Madden MC, Mehan RS (2010) Acute daily psychological stress causes increased atrophic gene expression and myostatin-dependent muscle atrophy. Am J Physiol Regul Integr Comp Physiol 299: R889-R898. doi:10.1152/ajpregu.00296.2010. PubMed: 20592178.
[43]  Bauer ME, Perks P, Lightman SL, Shanks N (2001) Restraint stress is associated with changes in glucocorticoid immunoregulation. Physiol Behav 73: 525-532. doi:10.1016/S0031-9384(01)00503-0. PubMed: 11495656.
[44]  Kinsey SG, Bailey MT, Sheridan JF, Padgett DA, Avitsur R (2007) Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Brain Behav Immun 21: 458-466. doi:10.1016/j.bbi.2006.11.001. PubMed: 17178210.
[45]  Landmark-H?yvik H, Reinertsen KV, Loge JH, Foss? SD, B?rresen-Dale AL et al. (2009) Alterations of gene expression in blood cells associated with chronic fatigue in breast cancer survivors. Pharmacogenomics J 9: 333-340. doi:10.1038/tpj.2009.27. PubMed: 19546881.
[46]  Kelly JJ, Martin A, Whitworth JA (2000) Role of erythropoietin in cortisol-induced hypertension. J Hum Hypertens 14: 195-198. doi:10.1038/sj.jhh.1000959. PubMed: 10694834.
[47]  Wei C, Zhou J, Huang X, Li M (2008) Effects of psychological stress on serum iron and erythropoiesis. Int J Hematol 88: 52-56. doi:10.1007/s12185-008-0105-4. PubMed: 18543064.
[48]  Li Y, Zheng Y, Qian J, Chen X, Shen Z et al. (2012) Preventive effects of zinc against psychological stress-induced iron dyshomeostasis, erythropoiesis inhibition, and oxidative stress status in rats. Biol Trace Elem Res 147: 285-291. doi:10.1007/s12011-011-9319-z. PubMed: 22274754.
[49]  Ganguli G, Back J, Sengupta S, Wasylyk B (2002) The p53 tumour suppressor inhibits glucocorticoid-induced proliferation of erythroid progenitors. EMBO Rep 3: 569-574. doi:10.1093/embo-reports/kvf114. PubMed: 12034755.
[50]  Kerenyi MA, Orkin SH (2010) Networking erythropoiesis. J Exp Med 207: 2537-2541. doi:10.1084/jem.20102260. PubMed: 21098097.
[51]  Laakko T, Fraker P (2002) Rapid changes in the lymphopoietic and granulopoietic compartments of the marrow caused by stress levels of corticosterone. Immunology 105: 111-119. doi:10.1046/j.1365-2567.2002.01346.x. PubMed: 11849321.
[52]  Trottier MD, Newsted MM, King LE, Fraker PJ (2008) Natural glucocorticoids induce expansion of all developmental stages of murine bone marrow granulocytes without inhibiting function. Proc Natl Acad Sci U S A 105: 2028-2033. doi:10.1073/pnas.0712003105. PubMed: 18250324.
[53]  McConnell BB, Yang VW (2010) Mammalian kruppel-like factors in health and diseases. Physiol Rev 90: 1337-1381. doi:10.1152/physrev.00058.2009. PubMed: 20959618.
[54]  Quadrini KJ, Gruzglin E, Bieker JJ (2008) Non-random subcellular distribution of variant EKLF in erythroid cells. Exp Cell Res 314: 1595-1604. doi:10.1016/j.yexcr.2008.01.033. PubMed: 18329016.
[55]  Siatecka M, Bieker JJ (2011) The multifunctional role of EKLF/KLF1 during erythropoiesis. Blood 118: 2044-2054. doi:10.1182/blood-2011-03-331371. PubMed: 21613252.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133