Circulating angiogenic cell function is inhibited by cortisol in vitro and associated with psychological stress and cortisol in vivo

Psychoneuroendocrinology

Volumn 67, Issue , 2016, Pages 216-223

  Aschbacher, Kirstin ^a,b   Derakhshandeh, Ronak ^a   Flores, Abdiel J ^c   Narayan, Shilpa ^a   Mendes, Wendy Berry ^a   Springer, Matthew L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Institute for Integrative Health   (United States)

^c Columbia University ^*  (United States)

Author keywords

Angiogenesis; Anxiety; Circulating hematopoietic progenitor cells; Endothelial progenitor cells; Executive function; Sustained attention

Indexed keywords

HYDROCORTISONE; MIFEPRISTONE; VASCULOTROPIN; VASCULOTROPIN A;

ADULT; AFRICAN AMERICAN; ARTICLE; ATTENTION; BLOOD SAMPLING; CARDIOVASCULAR PARAMETERS; CARDIOVASCULAR RISK; CELL FUNCTION; CELL ISOLATION; CELL MIGRATION; CIRCULATING ANGIOGENIC CELL; ENDOTHELIUM CELL; EXECUTIVE FUNCTION; FEMALE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IN VITRO STUDY; IN VIVO STUDY; MALE; MENTAL STRESS; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SALIVA ANALYSIS; SOCIAL BEHAVIOR; SOCIAL STRESS; THREAT; ANTAGONISTS AND INHIBITORS; ANXIETY; CELL CULTURE; CELL MIGRATION ASSAY; CELL MOTION; DRUG EFFECTS; ENDOTHELIAL PROGENITOR CELL; FEAR; INDIVIDUALITY; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; SALIVA; YOUNG ADULT;

ADULT; AFRICAN AMERICANS; ANXIETY; ATTENTION; CELL MIGRATION ASSAYS; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIAL PROGENITOR CELLS; FEAR; FEMALE; HUMANS; HYDROCORTISONE; INDIVIDUALITY; MALE; MIFEPRISTONE; SALIVA; STRESS, PSYCHOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A; YOUNG ADULT;

EID: 84959159467     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2016.02.019     Document Type: Article

References (55)

1. Adam E.K., Vrshek-Schallhorn S., Kendall A.D., Mineka S., Zinbarg R.E., Craske M.G. Prospective associations between the cortisol awakening response and first onsets of anxiety disorders over a six-year follow-up-2013 Curt Richter Award Winner. Psychoneuroendocrinology 2014, 44:47-59. 10.1016/j.psyneuen.2014.02.014.
2. Aschbacher K., Chen Q., Varga M., Haddad D., Yeghiazarians Y., Epel E., Wolkowitz O.M., Springer M.L. Higher fasting glucose levels are associated with reduced circulating angiogenic cell migratory capacity among healthy individuals. Am. J. Cardiovasc. Dis 2012, 12-19.
3. Aschbacher K., Epel E., Wolkowitz O.M., Prather A., Puterman E., Dhabhar F. Maintenance of a positive outlook during acute stress protects against pro-inflammatory reactivity and future depressive symptoms. Brain Behav. Immun. 2012, 26:346-352. 10.1016/j.bbi.2011.10.010.
4. Aschbacher K., O'Donovan A., Wolkowitz O.M., Dhabhar F.S., Su Y., Epel E. Good stress, bad stress and oxidative stress: insights from anticipatory cortisol reactivity. Psychoneuroendocrinology 2013, 38:1698-1708. 10.1016/j.psyneuen.2013.02.004.
5. Aschbacher K., Rodriguez-Fernandez M., van Wietmarschen H., Tomiyama A.J., Jain S., Epel E., Doyle F.J., van der Greef J. The hypothalamic-pituitary-adrenal-leptin axis and metabolic health: a systems approach to resilience, robustness and control. Interface Focus 2014, 2014:0020.
6. Bellingrath S., Rohleder N., Kudielka B.M. Effort-reward-imbalance in healthy teachers is associated with higher LPS-stimulated production and lower glucocorticoid sensitivity of interleukin-6 in vitro. Biol. Psychol. 2013, 92:403-409. 10.1016/j.biopsycho.2012.12.003.
7. Chen H., Yiu K.H., Tse H.F. Relationships between vascular dysfunction, circulating endothelial progenitor cells, and psychological status in healthy subjects. Depress Anxiety 2011, 28:719-727. 10.1002/da.20839.
8. Chen Q., Varga M., Wang X., Haddad D.J., An S., Medzikovic L., Derakhshandeh R., Kostyushev D.S., Zhang Y., Clifford B.T., Luu E., Danforth O.M., Rafikov R., Gong W., Black S.M., Suchkov S.V., Fineman J.R., Heiss C., Aschbacher K., Yeghiazarians Y., Springer M.L. Overexpression of nitric oxide synthase restores circulating angiogenic cell function in patients with coronary artery disease: Implications for autologous cell therapy for myocardial infarction. JAHA 2016, 115:002257.
9. Chida Y., Steptoe A. Cortisol awakening response and psychosocial factors: a systematic review and meta-analysis. Biol. Psychol. 2009, 80:265-278. 10.1016/j.biopsycho.2008.10.004.
10. Clow A., Hucklebridge F., Stalder T., Evans P., Thorn L. The cortisol awakening response: more than a measure of HPA axis function. Neurosci. Biobehav. Rev. 2010, 35:97-103. S0149-7634(09)00208-5. 10.1016/j.neubiorev.2009.12.011.
11. Di Santo S., Yang Z., Wyler von Ballmoos M., Voelzmann J., Diehm N., Baumgartner I., Kalka C. Novel cell-free strategy for therapeutic angiogenesis: in vitro generated conditioned medium can replace progenitor cell transplantation. PLoS One 2009, e5643. 10.1371/journal.pone.0005643.
12. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 2004, 130:355-391. 2004-13724-001. 10.1037/0033-2909.130.3.355.
13. Dressendorfer R.A., Kirschbaum C., Rohde W., Stahl F., Strasburger C.J. Synthesis of a cortisol-biotin conjugate and evaluation as a tracer in an immunoassay for salivary cortisol measurement. J. Steroid Biochem. Mol. Biol. 1992, 43:683-692. 10.1016/0960-0760(92)90294-S.
14. Du J., Wang Y., Hunter R., Wei Y., Blumenthal R., Falke C., Khairova R., Zhou R., Yuan P., Machado-Vieira R., McEwen B.S., Manji H.K. Dynamic regulation of mitochondrial function by glucocorticoids. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3543-3548. 10.1073/pnas.0812671106.
15. Ebrecht M., Hextall J., Kirtley L.G., Taylor A., Dyson M., Weinman J. Perceived stress and cortisol levels predict speed of wound healing in healthy male adults. Psychoneuroendocrinology 2004, 29:798-809. 10.1016/S0306-4530(03)00144-6.
16. Eller N.H., Netterstrom B., Allerup P. Progression in intima media thickness-the significance of hormonal biomarkers of chronic stress. Psychoneuroendocrinology 2005, 30:715-723. 10.1016/j.psyneuen.2005.01.005.
17. Frantz S., Vincent K.A., Feron O., Kelly R.A. Innate immunity and angiogenesis. Circ. Res. 2005, 96:15-26. 10.1161/01.RES.0000153188.68898.ac.
18. Fries E., Dettenborn L., Kirschbaum C. The cortisol awakening response (CAR): facts and future directions. Int. J. Psychophysiol. 2009, 72:67-73. 10.1016/j.ijpsycho.2008.03.014.
19. Fuller-Rowell T.E., Doan S.N., Eccles J.S. Differential effects of perceived discrimination on the diurnal cortisol rhythm of African Americans and Whites. Psychoneuroendocrinology 2012, 37:107-118. 10.1016/j.psyneuen.2011.05.011.
20. Gillespie, C.D., Wigington, C., Hong, Y., Centers for Disease, C., Prevention, 2013. Coronary heart disease and stroke deaths-United States, 2009. Morbidity and mortality weekly report. Surveillance summaries 62 (Suppl. 3), 157-160.
21. Gupta K., Zhang J. Angiogenesis: a curse or cure?. Postgrad. Med. J. 2005, 81:236-242. 10.1136/pgmj.2004.023309.
22. Heiss C., Schanz A., Amabile N., Jahn S., Chen Q., Wong M.L., Rassaf T., Heinen Y., Cortese-Krott M., Grossman W., Yeghiazarians Y., Springer M.L. Nitric oxide synthase expression and functional response to nitric oxide are both important modulators of circulating angiogenic cell response to angiogenic stimuli. Arterioscler. Thromb. Vasc. Biol. 2010, 30:2212-2218. ATVBAHA.110.211581. 10.1161/ATVBAHA.110.211581.
23. Hirono K., Kemmotsu Y., Wittkowski H., Foell D., Saito K., Ibuki K., Watanabe K., Watanabe S., Uese K., Kanegane H., Origasa H., Ichida F., Roth J., Miyawaki T., Saji T. Infliximab reduces the cytokine-mediated inflammation but does not suppress cellular infiltration of the vessel wall in refractory Kawasaki disease. Pediatr. Res. 2009, 65:696-701. 10.1203/01.pdr.0000352115.41382.65, 10.1203/PDR.0b013e31819ed68d.
24. Hirschi K.K., Ingram D.A., Yoder M.C. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1584-1595. 10.1161/ATVBAHA.107.155960.
25. Holm P.W., Slart R.H., Zeebregts C.J., Hillebrands J.L., Tio R.A. Atherosclerotic plaque development and instability: a dual role for VEGF. Ann. Med. 2009, 41:257-264. 10.1080/07853890802516507.
26. Kalka C., Masuda H., Takahashi T., Kalka-Moll W.M., Silver M., Kearney M., Li T., Isner J.M., Asahara T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:3422-3427. 10.1073/pnas.070046397.
27. Keymel S., Kalka C., Rassaf T., Yeghiazarians Y., Kelm M., Heiss C. Impaired endothelial progenitor cell function predicts age-dependent carotid intimal thickening 2008, 103:582-586. 10.1007/s00395-008-0742-z.
28. Kiecolt-Glaser J.K., Loving T.J., Stowell J.R., Malarkey W.B., Lemeshow S., Dickinson S.L., Glaser R. Hostile marital interactions, proinflammatory cytokine production, and wound healing. Arch. Gen. Psychiatry 2005, 62:1377-1384. 10.1001/archpsyc.62.12.1377.
29. Kudielka B.M., Schommer N.C., Hellhammer D.H., Kirschbaum C. Acute HPA axis responses, heart rate, and mood changes to psychosocial stress (TSST) in humans at different times of day. Psychoneuroendocrinology 2004, 29:983-992.
30. Li Calzi S., Neu M.B., Shaw L.C., Kielczewski J.L., Moldovan N.I., Grant M.B. EPCs and pathological angiogenesis: when good cells go bad. Microvasc. Res. 2010, 79:207-216. 10.1016/j.mvr.2010.02.011.
31. Liu Y., Mladinov D., Pietrusz J.L., Usa K., Liang M. Glucocorticoid response elements and 11 beta-hydroxysteroid dehydrogenases in the regulation of endothelial nitric oxide synthase expression. Cardiovasc. Res. 2009, 81:140-147. cvn231 [pii]. 10.1093/cvr/cvn231.
32. Ma Z.L., Mai X.L., Sun J.H., Ju S.H., Yang X., Ni Y., Teng G.J. Inhibited atherosclerotic plaque formation by local administration of magnetically labeled endothelial progenitor cells (EPCs) in a rabbit model. Atherosclerosis 2009, 205:80-86. S0021-9150(08)00787-9 [pii]. 10.1016/j.atherosclerosis.2008.07.048.
33. Maner J.K., Miller S.L. Adaptive attentional attunement: perceptions of danger and attention to outgroup men. Soc. Cogn. 2013, 31:733-744. 10.1521/soco.2013.31.6.733.
34. Marrotte E.J., Chen D.D., Hakim J.S., Chen A.F. Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J. Clin. Invest. 2010, 120:4207-4219. 10.1172/JCI36858.
35. Mendes W.B., Blascovich J., Hunter S.B., Lickel B., Jost J.T. Threatened by the unexpected: physiological responses during social interactions with expectancy-violating partners. J. Pers. Soc. Psychol. 2007, 92:698-716. 2007-05059-009 [pii]. 10.1037/0022-3514.92.4.698.
36. Mendes W.B., Gray H.M., Mendoza-Denton R., Major B., Epel E.S. Why egalitarianism might be good for your health: physiological thriving during stressful intergroup encounters. Psychol. Sci. 2007, 18:991-998. PSCI2014 [pii]. 10.1111/j.1467-9280.2007.02014.x.
37. Mendes W.B., Major B., McCoy S., Blascovich J. How attributional ambiguity shapes physiological and emotional responses to social rejection and acceptance. J. Pers. Soc. Psychol. 2008, 94:278-291. 2008-00466-007 [pii]. 10.1037/0022-3514.94.2.278.
38. Miller G.E., Chen E., Sze J., Marin T., Arevalo J.M., Doll R., Ma R., Cole S.W. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-kappaB signaling. Biol. Psychiatry 2008, 64:266-272. S0006-3223(08)00361-2 [pii]. 10.1016/j.biopsych.2008.03.017.
39. O'Loughlin A., Kulkarni M., Vaughan E.E., Creane M., Liew A., Dockery P., Pandit A., O'Brien T. Autologous circulating angiogenic cells treated with osteopontin and delivered via a collagen scaffold enhance wound healing in the alloxan-induced diabetic rabbit ear ulcer model. Stem. Cell Res. Ther. 2013, 4:158. 10.1186/scrt388.
40. Ohtsuka M., Sasaki K., Ueno T., Seki R., Nakayoshi T., Koiwaya H., Toyama Y., Yokoyama S., Mitsutake Y., Chibana H., Itaya N., Okamura T., Imaizumi T. Platelet-derived microparticles augment the adhesion and neovascularization capacities of circulating angiogenic cells obtained from atherosclerotic patients. Atherosclerosis 2013, 227:275-282. 10.1016/j.atherosclerosis.2013.01.040.
41. Pober J.S., Sessa W.C. Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 2007, 7:803-815. 10.1038/nri2171.
42. Pruessner M., Hellhammer D.H., Pruessner J.C., Lupien S.J. Self-reported depressive symptoms and stress levels in healthy young men: associations with the cortisol response to awakening. Psychosom. Med. 2003, 65:92-99. 10.1097/01.PSY.0000040950.22044.10.
43. Rehman J., Li J., Orschell C.M., March K.L. Peripheral blood endothelial progenitor cells are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003, 107:1164-1169. 10.1161/01.CIR.0000058702.69484.A0.
44. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89. 10.1210/edrv.21.1.0389.
45. Sonnenschein K., Horvath T., Mueller M., Markowski A., Siegmund T., Jacob C., Drexler H., Landmesser U. Exercise training improves in vivo endothelial repair capacity of early endothelial progenitor cells in subjects with metabolic syndrome. Eur. J. Cardiovasc. Prev. Rehabil. 2011, 1741826710389373 [pii]. 10.1177/1741826710389373.
46. Thum T., Fraccarollo D., Schultheiss M., Froese S., Galuppo P., Widder J.D., Tsikas D., Ertl G., Bauersachs J. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 2007, 56:666-674. 56/3/666 [pii]. 10.2337/db06-0699.
47. Titchenell P.M., Antonetti D.A. Using the past to inform the future: anti-VEGF therapy as a road map to develop novel therapies for diabetic retinopathy. Diabetes 2013, 62:1808-1815. 10.2337/db12-1744.
48. Toyama Y., Sasaki K., Tachibana K., Ueno T., Kajimoto H., Yokoyama S., Ohtsuka M., Koiwaya H., Nakayoshi T., Mitsutake Y., Chibana H., Itaya N., Imaizumi T. Ultrasound stimulation restores impaired neovascularization-related capacities of human circulating angiogenic cells. Cardiovasc. Res. 2012, 95:448-459. 10.1093/cvr/cvs173.
49. Van Craenenbroeck E.M., Denollet J., Paelinck B.P., Beckers P., Possemiers N., Hoymans V.Y., Vrints C.J., Conraads V.M. Circulating CD34+/KDR+ endothelial progenitor cells are reduced in chronic heart failure patients as a function of Type D personality. Clin. Sci. 2009, 117:165-172. CS20080564 [pii]. 10.1042/CS20080564.
50. Van Craenenbroeck E.M., Hoymans V.Y., Beckers P.J., Possemiers N.M., Wuyts K., Paelinck B.P., Vrints C.J., Conraads V.M. xercise training improves function of circulating angiogenic cells in patients with chronic heart failure. Basic Res. Cardiol. 2010, 105:665-676. 10.1007/s00395-010-0105-4.
51. Vasa M., Fichtlscherer S., Aicher A., Adler K., Urbich C., Martin H., Zeiher A.M., Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ. Res. 2001, 89:E1-E7. 10.1161/hh1301.093953.
52. Vogelzangs N., Beekman A.T., Milaneschi Y., Bandinelli S., Ferrucci L., Penninx B.W. Urinary cortisol and six-year risk of all-cause and cardiovascular mortality. J. Clin. Endocrinol. Metab. 2010, 95:4959-4964. jc. 2010-0192 [pii]. 10.1210/jc.2010-0192.
53. Vrshek-Schallhorn S., Doane L.D., Mineka S., Zinbarg R.E., Craske M.G., Adam E.K. The cortisol awakening response predicts major depression: predictive stability over a 4-year follow-up and effect of depression history. Psychol. Med. 2013, 43:483-493.
54. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. J. Pers. Soc. Psychol. 1988, 54:1063-1070. 10.1037/0022-3514.54.6.1063.
55. Yusuf S., Hawken S., Ounpuu S., Dans T., Avezum A., Lanas F., McQueen M., Budaj A., Pais P., Varigos J., Lisheng L. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 2004, 364:937-952. S0140-6736(04)17018-9 [pii]. 10.1016/S0140-6736(04)17018-9.