Immunophenotypic alterations in resident immune cells and myocardial fibrosis in the aging rhesus macaque (Macaca mulatta) heart

Toxicologic Pathology

Volumn 40, Issue 4, 2012, Pages 637-646

  MacRi, Sheila C ^a   Bailey, Charles C ^a   De Oca, Nicole Monts ^a   Silva, Nilsa A ^a   Rosene, Douglas L ^b   Mansfield, Keith G ^c   Miller, Andrew D ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

aging; cardiac fibrosis; dendritic cell; immunohistochemistry; lymphocyte; macrophage; rhesus macaque

Indexed keywords

CD163 ANTIGEN;

AGING; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITIC CELL; HEART MUSCLE FIBROSIS; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; IMMUNOPHENOTYPING; MACACA MULATTA; MACROPHAGE; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

AGING; ANIMALS; ANTIGENS, CD; DENDRITIC CELLS; FIBROSIS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; MACACA MULATTA; MACROPHAGES; MYOCARDIUM; STATISTICS, NONPARAMETRIC; T-LYMPHOCYTES;

MACACA; MACACA MULATTA;

EID: 84861812495     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623311436177     Document Type: Article

References (46)

1. Allessie M., Schotten U., Verheule S., Harks E.. Gene therapy for repair of cardiac fibrosis: A long way to Tipperary. Circulation. 2005 ; 111: 391-3
2. Anderson K. R., Sutton M. G., Lie J. T.. Histopathological types of cardiac fibrosis in myocardial disease. J Pathol. 1979 ; 128: 79-85
3. Appt S. E., Ethun K. F.. Reproductive aging and risk for chronic disease: Insights from studies of nonhuman primates. Maturitas. 2010 ; 67: 7-14
4. Boyle A. J., Shih H., Hwang J., Ye J., Lee B., Zhang Y., Kwon D., Jun K., Zheng D., Sievers R., Angeli F., Yeghiazarians Y., Lee R. Cardiomyopathy of aging in the mammalian heart is characterized by myocardial hypertrophy, fibrosis and a predisposition towards cardiomyocyte apoptosis and autophagy. Exp Gerontol. 2011 ; 45: 549-59
5. Chamanza R., Parry N. M., Rogerson P., Nicol J. R., Bradley A. E.. Spontaneous lesions of the cardiovascular system in purpose-bred laboratory nonhuman primates. Toxicol Pathol. 2006 ; 34: 357-63
6. Chen W., Frangogiannis N. G.. The role of inflammatory and fibrogenic pathways in heart failure associated with aging. Heart Fail Rev. 2010 ; 15: 415-22
7. Cieslik K. A., Taffet G. E., Carlson S., Hermosillo J., Trial J., Entman M. L.. Immune-inflammatory dysregulation modulates the incidence of progressive fibrosis and diastolic stiffness in the aging heart. J Mol Cell Cardiol. 2011 ; 50: 248-56
8. Clarkson T. B., Prichard R. W., Morgan T. M., Petrick G. S., Klein K. P.. Remodeling of coronary arteries in human and nonhuman primates. JAMA. 1994 ; 271: 289-94
9. de Jong S V. T, van Rijen H. V. M., de Bakker J. M. T. Fibrosis and cardiac arrhythmias. Journal of Cardiovascular Pharmacology. 2011 ; 57: 630-38
10. de Souza R. R.. Aging of myocardial collagen. Biogerontology. 2002 ; 3: 325-35
11. Debessa M. L., de Souza R. R.. Age related changes of the collagen network of the human heart. Mechanisms of Ageing and Development. 2001 ; 122: 1049-58
12. Dobaczewski M., Bujak M., Zymek P., Ren G., Entman M. L., Frangogiannis N. G.. Extracellular matrix remodeling in canine and mouse myocardial infarcts. Cell Tissue Res. 2006 ; 324: 475-88
13. Ely J. J., Bishop M. A., Lammey M. L., Sleeper M. M., Steiner J. M., Lee D. R.. Use of biomarkers of collagen types I and III fibrosis metabolism to detect cardiovascular and renal disease in chimpanzees (Pan troglodytes). Comp Med. 2010 ; 60: 154-8
14. Frangogiannis N. G.. The immune system and cardiac repair. Pharmacological Research. 2008 ; 58: 88-111
15. Frangogiannis N. G., Mendoza L. H., Ren G., Akrivakis S., Jackson P. L., Michael L. H., Smith C. W., Entman M. L.. MCSF expression is induced in healing myocardial infarcts and may regulate monocyte and endothelial cell phenotype. Am J Physiol Heart Circ Physiol. 2003 ; 285: H483-92
16. Geijtenbeek T. B., Torensma R., van Vliet S. J., van Duijnhoven G. C., Adema G. J., van Kooyk Y., Figdor C. G.. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 2000 ; 100: 575-85
17. Goumans M. J., van Zonneveld A. J., ten Dijke P.. Transforming growth factor beta-induced endothelial-to-mesenchymal transition: A switch to cardiac fibrosis?. Trends Cardiovasc Med. 2008 ; 18: 293-8
18. Hinglais N., Heudes D., Nicoletti A., Mandet C., Laurent M., Bariety J., Michel J. B.. Colocalization of myocardial fibrosis and inflammatory cells in rats. Lab Invest. 1994 ; 70: 286-94
19. Keenan C. M., Vidal J. D.. Standard morphologic evaluation of the heart in the laboratory dog and monkey. Toxicol Pathol. 2006 ; 34: 67-74
20. Krenning G., Zeisberg E. M., Kalluri R.. The origin of fibroblasts and mechanism of cardiac fibrosis. J Cell Physiol. 2010 ; 225: 631-7
21. Kumar V. A. A., Fausto N., Aster J. C. Robbins and Cotran Pathologic Basis of Disease. Philadelphia, PA.: Saunders ; 2010 :
22. Kvakan H., Kleinewietfeld M., Qadri F., Park J. K., Fischer R., Schwarz I., Rahn H. P., Plehm R., Wellner M., Elitok S., Gratze P., Dechend R., Luft F. C., Muller D. N.. Regulatory T cells ameliorate angiotensin II-induced cardiac damage. Circulation. 2009 ; 119: 2904-12
23. Lammey M. L., Baskin G. B., Gigliotti A. P., Lee D. R., Ely J. J., Sleeper M. M.. Interstitial myocardial fibrosis in a captive chimpanzee (Pan troglodytes) population. Comp Med. 2008 ; 58: 389-94
24. Leong C. K., Leong F. J. W. M. Manual of Diagnostic Antibodies for Immunohistology. London: Greenwich Medical Media Ltd. ; 2003 :
25. Lowenstine L. J.. A primer of primate pathology: Lesions and nonlesions. Toxicol Pathol. 2003 ; 31 ((Suppl.)). 92-102
26. Moriwaki H., Stempien-Otero A., Kremen M., Cozen A. E., Dichek D. A.. Overexpression of urokinase by macrophages or deficiency of plasminogen activator inhibitor type 1 causes cardiac fibrosis in mice. Circ Res. 2004 ; 95: 637-44
27. Mosser D. M.. The many faces of macrophage activation. J Leukoc Biol. 2003 ; 73: 209-12
28. Mosser D. M., Edwards J. P.. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008 ; 8: 958-69
29. Park M., Shen Y. T., Gaussin V., Heyndrickx G. R., Bartunek J., Resuello R. R., Natividad F. F., Kitsis R. N., Vatner D. E., Vatner S. F.. Apoptosis predominates in nonmyocytes in heart failure. Am J Physiol Heart Circ Physiol. 2009 ; 297: H785-91
30. Pick R., Janicki J. S., Weber K. T.. Myocardial fibrosis in nonhuman primate with pressure overload hypertrophy. Am J Pathol. 1989 ; 135: 771-81
31. Qureshi S. R.. Chronic interstitial myocarditis in primates. Vet Pathol. 1979 ; 16: 486-7
32. Randolph G. J., Ochando J., Partida-Sanchez S.. Migration of dendritic cell subsets and their precursors. Annu Rev Immunol. 2008 ; 26: 293-316
33. Roth G. S., Mattison J. A., Ottinger M. A., Chachich M. E., Lane M. A., Ingram D. K.. Aging in rhesus monkeys: Relevance to human health interventions. Science. 2004 ; 305: 1423-6
34. Vidal J. D., Drobatz L. S., Holliday D. F., Geiger L. E., Thomas H. C.. Spontaneous findings in the heart of Mauritian-origin cynomolgus macaques (Macaca fascicularis). Toxicol Pathol. 2010 ; 38: 297-302
35. Weber K. T., Janicki J. S., Shroff S. G., Pick R., Chen R. M., Bashey R. I.. Collagen remodeling of the pressure-overloaded, hypertrophied nonhuman primate myocardium. Circ Res. 1988 ; 62: 757-65
36. Weber K. T., Pick R., Jalil J. E., Janicki J. S., Carroll E. P.. Patterns of myocardial fibrosis. J Mol Cell Cardiol. 1989 ; 21 (Suppl 5). 121-31
37. Wei L.. Immunological aspect of cardiac remodeling: T lymphocyte subsets in inflammation-mediated cardiac fibrosis. Exp Mol Pathol. 2011 ; 90: 74-8
38. Wynn T. A.. Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol. 2004 ; 4: 583-94
39. Wynn T. A.. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest. 2007 ; 117: 524-9
40. Wynn T. A.. Cellular and molecular mechanisms of fibrosis. J Pathol. 2008 ; 214: 199-210
41. Yano T., Miura T., Whittaker P., Miki T., Sakamoto J., Nakamura Y., Ichikawa Y., Ikeda Y., Kobayashi H., Ohori K., Shimamoto K.. Macrophage colony-stimulating factor treatment after myocardial infarction attenuates left ventricular dysfunction by accelerating infarct repair. J Am Coll Cardiol. 2006 ; 47: 626-34
42. Yearley J. H., Mansfield K. G., Carville A. A., Sokos G. G., Xia D., Pearson C. B., Shannon R. P.. Antigenic stimulation in the simian model of HIV infection yields dilated cardiomyopathy through effects of TNFalpha. AIDS. 2008 ; 22: 585-94
43. Yearley J. H., Pearson C., Shannon R. P., Mansfield K. G.. Phenotypic variation in myocardial macrophage populations suggests a role for macrophage activation in SIV-associated cardiac disease. AIDS Res Hum Retroviruses. 2007 ; 23: 515-24
44. Yu Q., Horak K., Larson D. F.. Role of T lymphocytes in hypertension-induced cardiac extracellular matrix remodeling. Hypertension. 2006 ; 48: 98-104
45. Yu Q., Vazquez R., Zabadi S., Watson R. R., Larson D. F.. T-lymphocytes mediate left ventricular fibrillar collagen cross-linking and diastolic dysfunction in mice. Matrix Biol. 2010 ; 29: 511-8
46. Zabka T. S., Irwin M., Albassam M. A.. Spontaneous cardiomyopathy in cynomolgus monkeys (Macaca fascicularis). Toxicol Pathol. 2009 ; 37: 814-8