Journal of Cardiac Failure
Volume 15, Issue 7 , Pages 607-615 , September 2009

A Potential Shift From Adaptive Immune Activity to Nonspecific Inflammatory Activation Associated With Higher Depression Symptoms in Chronic Heart Failure Patients

  • Laura S. Redwine, PhD

      Affiliations

    • Department of Psychiatry, University of California, San Diego, La Jolla, CA
    • Department of Medicine, University of California, San Diego, La Jolla, CA
    • Corresponding Author InformationReprint requests: Dr. Laura S. Redwine, University of California, San Diego, Departments of Psychiatry and Medicine, La Jolla, CA 92161. Tel: (858) 552-8585 x5359.
    • ,
  • Petra H. Wirtz, PhD

      Affiliations

    • Department of Clinical Psychology and Psychotherapy, Psychological Institute, University of Zurich, Zurich, Switzerland
    • ,
  • Suzi Hong, PhD

      Affiliations

    • Department of Psychiatry, University of California, San Diego, La Jolla, CA
    • ,
  • Ines Pandzic, BS

      Affiliations

    • Department of Medicine, University of California, San Diego, La Jolla, CA
    • ,
  • Stephanie Cammarata, BS

      Affiliations

    • Department of Medicine, University of California, San Diego, La Jolla, CA
    • ,
  • Joseph Tafur, MD

      Affiliations

    • Department of Psychiatry, University of California, San Diego, La Jolla, CA
    • ,
  • Steven M. Carter, BS

      Affiliations

    • Department of Medicine, University of California, San Diego, La Jolla, CA
    • ,
  • Barry Greenberg, MD

      Affiliations

    • Department of Medicine, University of California, San Diego, La Jolla, CA
    • ,
  • Paul J. Mills, PhD

      Affiliations

    • Department of Psychiatry, University of California, San Diego, La Jolla, CA

Received 14 October 2008 ,Revised 21 January 2009 ,Accepted 26 January 2009.

References 

  1. Jiang W, Kuchibhatla M, Cuffe MS, Christopher EJ, Alexander JD, Clary GL, et al. Prognostic value of anxiety and depression in patients with chronic heart failure. Circulation. 2004;110:3452–3456
  2. Sullivan M, Levy WC, Russo JE, Spertus JA. Depression and health status in patients with advanced heart failure: a prospective study in tertiary care. J Card Fail. 2004;10:390–396
  3. Junger J, Schellberg D, Muller-Tasch T, Raupp G, Zugck C, Haunstetter A, et al. Depression increasingly predicts mortality in the course of congestive heart failure. Eur J Heart Fail. 2005;7:261–267
  4. Rutledge T, Reis VA, Linke SE, Greenberg BH, Mills PJ. Depression in heart failure a meta-analytic review of prevalence, intervention effects, and associations with clinical outcomes. J Am Coll Cardiol. 2006;48:1527–1537
  5. Sherwood A, Blumenthal JA, Trivedi R, Johnson KS, O'Connor CM, Adams KF, et al. Relationship of depression to death or hospitalization in patients with heart failure. Arch Intern Med. 2007;167:367–373
  6. Irwin M, Thompson J, Miller C, Gillin JC, Ziegler M. Effects of sleep and sleep deprivation on catecholamine and interleukin-2 levels in humans: clinical implications. J Clin Endocrinol Metab. 1999;84:1979–1985
  7. Moorman AJ, Mozaffarian D, Wilkinson CW, Lawler RL, McDonald GB, Crane BA, et al. In patients with heart failure elevated soluble TNF-receptor 1 is associated with higher risk of depression. J Card Fail. 2007;13:738–743
  8. Lesperance F, Frasure-Smith N, Theroux P, Irwin M. The association between major depression and levels of soluble intercellular adhesion molecule 1, interleukin-6, and C-reactive protein in patients with recent acute coronary syndromes. Am J Psychiatry. 2004;161:271–277
  9. Miller GE, Freedland KE, Carney RM. Depressive symptoms and the regulation of proinflammatory cytokine expression in patients with coronary heart disease. J Psychosom Res. 2005;59:231–236
  10. Suarez EC, Lewis JG, Krishnan RR, Young KH. Enhanced expression of cytokines and chemokines by blood monocytes to in vitro lipopolysaccharide stimulation are associated with hostility and severity of depressive symptoms in healthy women. Psychoneuroendocrinology. 2004;29:1119–1128
  11. Ferketich A, Ferguson JP, Binkley PF. Depressive symptoms and inflammation among heart failure patients. Am Heart J. 2005;150:132–136
  12. Whooley MA, Caska CM, Hendrickson BE, Rourke MA, Ho J, Ali S. Depression and inflammation in patients with coronary heart disease: findings from the Heart and Soul Study. Biol Psychiatry. 2007;62:314–320
  13. Lanquillon S, Krieg JC, Bening-Abu-Shach U, Vedder H. Cytokine production and treatment response in major depressive disorder. Neuropsychopharmacology. 2000;22:370–379
  14. Zorrilla EP, Luborsky L, McKay JR, Rosenthal R, Houldin A, Tax A, et al. The relationship of depression and stressors to immunological assays: a meta-analytic review. Brain Behav Immun. 2001;15:199–226
  15. Waldman WJ, Williams MV, Lemeshow S, Binkley P, Guttridge D, Kiecolt-Glaser JK, et al. Epstein-Barr virus-encoded dUTPase enhances proinflammatory cytokine production by macrophages in contact with endothelial cells: evidence for depression-induced atherosclerotic risk. Brain Behav Immun. 2008;22:215–223
  16. de Virginy D. Novel and potential future biomarkers for assessment of the severity and prognosis of chronic heart failure: a clinical review. Heart Fail Rev. 2006;11:333–334
  17. Mielniczuk LM, Baughman KL. Immune modulation therapy in heart failure. Congest Heart Fail. 2006;12:91–96quiz 97–98
  18. Reiche EM, Nunes SO, Morimoto HK. Stress, depression, the immune system, and cancer. Lancet Oncol. 2004;5:617–625
  19. Irwin M, Costlow C, Williams H, Artin KH, Chan CY, Stinson DL, et al. Cellular immunity to varicella-zoster virus in patients with major depression. J Infect Dis. 1998;178(Suppl 1):S104–S108
  20. Afanasyeva M, Georgakopoulos D, Belardi DF, Bedja D, Fairweather D, Wang Y, et al. Impaired up-regulation of CD25 on CD4+ T cells in IFN-gamma knockout mice is associated with progression of myocarditis to heart failure. Proc Natl Acad Sci. 2005;102:180–185
  21. Shimbo D, Chaplin W, Crossman D, Haas D, Davidson KW. Role of depression and inflammation in incident coronary heart disease events. Am J Cardiol. 2005;96:1016–1021
  22. Empana J, Sykes DH, Luc G, Juhan-Vague I, Arveiler D, Ferrieres J, et al. Contributions of depressive mood and circulating inflammatory markers to coronary heart disease in healthy European men: the Prospective Epidemiological Study of Myocardial Infarction (PRIME). Circulation. 2005;111:2299–2305
  23. Opasich C, Pacini F, Ambrosino N, Riccardi PG, Febo O, Ferrari R, et al. Sick euthyroid syndrome in patients with moderate-to-severe chronic heart failure. Eur Heart J. 1996;17:1860–1866
  24. Szabo MC, Butcher EC, McIntyre BW, Schall TJ, Bacon KB. RANTES stimulation of T lymphocyte adhesion and activation: role for LFA-1 and ICAM-3. Eur J Immunol. 1997;27:1061–1068
  25. Chen J, Fujimoto C, Vistica BP, He J, Wawrousek EF, Kelsall B, et al. Active participation of antigen-nonspecific lymphoid cells in immune-mediated inflammation. J Immunol. 2006;177:3362–3368
  26. Adamopoulos S, Parissis J, Kroupis C, Georgiadis M, Karatzas D, Karavolias G, et al Physical training reduces peripheral markers of inflammation in patients with chronic heart failure. Eur Heart J. 2001;22:791–797
  27. Pyo RT, Sui J, Dhume A, Palomeque J, Blaxall BC, Diaz G, et al. CXCR4 modulates contractility in adult cardiac myocytes. J Mol Cell Cardiol. 2006;41:834–844
  28. Frangogiannis NG, Dewald O, Xia Y, Ren G, Haudek S, Leucker T, et al. Critical role of monocyte chemoattractant protein-1/CC chemokine ligand 2 in the pathogenesis of ischemic cardiomyopathy. Circulation. 2007;115:584–592
  29. Linden W, Gerin W, Davidson K. Cardiovascular reactivity: status quo and a research agenda for the new millennium. Psychosom Med. 2003;65:5–8
  30. Kop WJ, Weissman NJ, Zhu J, Bonsall RW, Doyle M, Stretch MR, et al. Effects of acute mental stress and exercise on inflammatory markers in patients with coronary artery disease and healthy controls. Am J Cardiol. 2008;101:767–773
  31. Chung I, Goyal D, Macfadyen RJ, Lip GY. The effects of maximal treadmill graded exercise testing on haemorheological, haemodynamic and flow cytometry platelet markers in patients with systolic or diastolic heart failure. Eur J Clin Invest. 2008;38:150–158
  32. Pace TW, Mletzko TC, Alagbe O, Musselman DL, Nemeroff CB, Miller AH, et al. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am J Psychiatry. 2006;163:1630–1633
  33. O'Keeffe ST, Lye M, Donnellan C, Carmichael DN. Reproducibility and responsiveness of quality of life assessment and six minute walk test in elderly heart failure patients. Heart. 1998;80:377–382
  34. Redwine LS, Pert CB, Rone JD, Nixon R, Vance M, Sandler B, et al. Peptide T blocks GP120/CCR5 chemokine receptor-mediated chemotaxis. Clinical Immunol. 1999;93:124–131
  35. Batista ML, Santos RV, Cunha LM, Mattos K, Oliveira EM, Seelaender MC, et al. Changes in the pro-inflammatory cytokine production and peritoneal macrophage function in rats with chronic heart failure. Cytokine. 2006;34:284–290
  36. Zalai CV, Kolodziejczyk MD, Pilarski L, Christov A, Nation PN, Lundstrom-Hobman M, et al. Increased circulating monocyte activation in patients with unstable coronary syndromes. J Am Coll Cardiol. 2001;38:1340–1347
  37. Ding Z, Issekutz TB, Downey GP, Waddell TK. L-selectin stimulation enhances functional expression of surface CXCR4 in lymphocytes: implications for cellular activation during adhesion and migration. Blood. 2003;101:4245–4252
  38. Nanki T, Lipsk PE. Cutting edge: stromal cell-derived factor-1 is a costimulator for CD4+ T cell activation. J Immunol. 2000;164:5010–5014
  39. Vicente-Manzanaares M, Montoya MC, Mellado M, Frade JMR, del Pozo MA, Nieto M, et al. The chemokine SDF-1 alpha triggers a chemotactic response and induces cell polarization in human B lymphocytes. Eur J Immunol. 1998;28:2197–2207
  40. Redwine L, Snow S, Mills P, Irwin M. Acute psychological stress: effects on chemotaxis and cellular adhesion molecule expression. Psychosom Med. 2003;65:598–603
  41. Redwine L, et al. Differential immune cell chemotaxis responses to acute psychological stress in Alzheimer caregivers compared to non-caregiver controls. Psychosom Med. 2004;66:770–775
  42. Borg G. Perceived exertion as an indicator of somatic stress. Scand J Rehabil Med. 1970;2:92–98
  43. Hong S, Johnson TA, Farag NH, Guy HJ, Matthews SC, Ziegler MG, et al. Attenuation of T-lymphocyte demargination and adhesion molecule expression in response to moderate exercise in physically fit individuals. J Appl Physiol. 2005;98:1057–1063
  44. Hong S, Mills PJ. Effects of an exercise challenge on mobilization and surface marker expression of monocyte subsets in individuals with normal vs. elevated blood pressure. Brain Behav Immun. 2008;22:590–599
  45. Beck AT. Depression inventory. Philadelphia: Center for Cognitive Therapy; 1978;
  46. Beck AT, Steer RA, Ball R, Ranieri W. Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. J Pers Assess. 1996;67:588–597
  47. American Psychiatric Association . Diagnostic and Statistical Manual of Mental Disorders. 4th ed.. Washington DC: American Psychiatric Association; 1994;
  48. Baron RM, Kenny DA. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986;51:1173–1182
  49. Fairweather D, Frisancho-Kiss S, Yusung SA, Barrett MA, Davis SE, Gatewood SJ, et al. Interferon-gamma protects against chronic viral myocarditis by reducing mast cell degranulation, fibrosis, and the profibrotic cytokines transforming growth factor-beta 1, interleukin-1 beta, and interleukin-4 in the heart. Am J Pathol. 2004;165:1883–1894
  50. Bandura A. Health promotion by social cognitive means. Health Educ Behav. 2004;31:143–164
  51. Dadfar E, Jacobson SH, Lundahl J. Newly recruited human monocytes have a preserved responsiveness towards bacterial peptides in terms of CD11b up-regulation and intracellular hydrogen peroxide production. Clin Exp Immunol. 2007;148:573–582
  52. Luethviksson BR, Gunnlaugsdottir B. Transforming growth factor-beta as a regulator of site-specific T-cell inflammatory response. Scand J Immunol. 2003;58:129–138
  53. Stein JV, Nombela-Arrieta C. Chemokine control of lymphocyte trafficking: a general overview. Immunology. 2005;116:1–12
  54. Woo YJ, Grand TJ, Berry MF, Atluri P, Moise MA, Hsu VM, et al. Stromal cell-derived factor and granulocyte-monocyte colony-stimulating factor form a combined neovasculogenic therapy for ischemic cardiomyopathy. J Thorac Cardiovasc Surg. 2005;130:321–329
  55. Anderson CD, Heydarkhan-Hagvall S, Schenke-Layland K, Yang JQ, Jordan MC, Kim JK, et al. The role of cytoprotective cytokines in cardiac ischemia/reperfusion injury. J Surg Res. 2008;148:164–171
  56. Valgimigli M, Rigolin GM, Fucili A, Porta MD, Soukhomovskaia O, Malagutti P, et al. CD34+ and endothelial progenitor cells in patients with various degrees of congestive heart failure. Circulation. 2004;110:1209–1212
  57. Frantz S, Bauersachs J, Kelly RA. Innate immunity and the heart. Curr Pharm Des. 2005;11:1279–1290
  58. Wirtz PH, Hong S, Redwine LS, Tafur J, Rutledge T, Ziegler MG, et al. Depressive symptoms are associated with soluble p-selectin reactivity to acute exercise in heart failure. Biol Psychiatry. 2008;Dec; [Epub ahead of print]
  59. Sela U, Hershkoviz R, Cahalon L, Lider O, Mozes E. Down-regulation of stromal cell-derived factor-1alpha-induced T cell chemotaxis by a peptide based on the complementarity-determining region 1 of an anti-DNA autoantibody via up-regulation of TGF-beta secretion. J Immunol. 2005;174:302–309
  60. Debes GF, Dahl ME, Mahiny AJ, Bonhagen K, Campbell DJ, Siegmund K, et al. Chemotactic responses of IL-4-, IL-10-, and IFN-gamma-producing CD4+ T cells depend on tissue origin and microbial stimulus. J Immunol. 2006;176:557–566
  61. Pavon L, Sandoval-Lopez G, Hernandez M, Loria F, Estrada I, Perez M, et al. Th2 cytokine response in major depressive disorder patients before treatment. J Neuroimmunol. 2006;172:156–165
  62. Kim YK, Na KS, Shin KH, Jung HY, Choi SH, Kim JB. Cytokine imbalance in the pathophysiology of major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2007;31:1044–1053
  63. Redwine L, Mills PJ, Hong S, Rutledge T, Reis V, Maisel A, et al. Cardiac-related hospitalization and/or death associated with immune dysregulation and symptoms of depression in heart failure patients. Psychosom Med. 2007;69:23–29
  64. Miller G, Freedland KE, Carney RM. Depressive symptoms and the regulation of proinflammatory cytokine expression in patients with coronary heart disease. J Psychosom Res. 2005;59:231–236
  65. Straub RH, Mayer M, Kreutz M, Leeb S, Scholmerich J, Falk W. Neurotransmitters of the sympathetic nerve terminal are powerful chemoattractants for monocytes. J Leukoc Biol. 2000;67:553–558
  66. Garcia JJ, del Carmen Saez M, De la Fuente M, Ortega E. Regulation of phagocytic process of macrophages by noradrenaline and its end metabolite 4-hydroxy-3-metoxyphenyl-glycol. Role of alpha- and beta-adrenoreceptors. Mol Cell Biochem. 2003;254:299–304

 Supported by grants HL-073355 and HL-57265 from the National Institutes of Health and IZKOBO-122843/1 by the Swiss National Foundation.

PII: S1071-9164(09)00033-5

doi: 10.1016/j.cardfail.2009.01.011

Journal of Cardiac Failure
Volume 15, Issue 7 , Pages 607-615 , September 2009

Article Tools

* Image Usage & Resolution