The Effect of Social Environment on Markers of Vascular Oxidative Stress and Inflammation in the Watanabe Heritable Hyperlipidemic Rabbit
Abstract
OBJECTIVE: Previous research demonstrated that social environment can influence progression of atherosclerosis in the Watanabe Heritable Hyperlipidemic (WHHL) rabbit. This study examined the effect of social environment on markers of oxidative stress and inflammation to clarify the physiological pathways potentially responsible for the influence of social environment on disease. METHODS AND RESULTS: WHHL rabbits were assigned to 1 of 3 social groups: an unstable group, in which unfamiliar rabbits were paired daily, with the pairing switched each week; a stable group, in which littermates were paired daily; and an individually-caged group. The stable group engaged in more affiliative social behavior than the unstable group. The unstable group showed more agonistic behavior compared with the stable group and higher C-reactive protein levels than the individually caged group. The individually caged group was behaviorally sedentary, had higher 24-hour urinary catecholamine levels than the other groups, and exhibited higher NAD(P)H-oxidase activity in the aortic arch relative to the stable group. CONCLUSIONS: The results suggest that social environment creates distinct behavioral contexts that can affect markers of inflammation and oxidative stress early in the development of atherosclerosis. Specifically, physical inactivity associated with individual caging affects indices of oxidative stress and inflammation. These pathophysiological markers may help to explain behaviorally related differences in the extent of atherosclerosis observed in prior studies.
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Social isolation increases 24-hour urinary catecholamines and evidence of oxidative stress in the aortic arch of Watanabe heritable hyperlipidemic rabbits.
“increases the 24 hour urinary catecholamines levels and evidence of oxidative stress in the aortic arch of the Watanabe heritable hyperlipidemic rabbit;19”
From Social isolation (2011) · cites this paper as [19]
Cites
Inflammation and Atherosclerosis
Libby, P., Ridker, P. M., & Maseri, A. (2002) · Circulation · doi:10.1161/hc0902.104353 · Cited by 7,724 · see citing works
Danesh, J., Wheeler, J. G., Hirschfield, G. M., Eda, S., Eiriksdottir, G., Rumley, A., Lowe, G. D. O., Pepys, M. B., & Gudnason, V. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa032804 · Cited by 2,953 · see citing works
Hypercholesterolemia increases endothelial superoxide anion production.
Ohara, Y., Peterson, T. E., & Harrison, D. G. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116491 · Cited by 1,765 · see citing works
The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases
Cai, H., Griendling, K. K., & Harrison, D. G. (2003) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(03)00233-5 · Cited by 687 · see citing works
Increased NADH-Oxidase–Mediated Superoxide Production in the Early Stages of Atherosclerosis
Warnholtz, A., Nickenig, G., Schulz, E., Macharzina, R. R., Bräsen, J. H., Skatchkov, M. P., Heitzer, T. A., Stasch, J. P., Griendling, K. K., Harrison, D. G., et al. (1999) · Circulation · doi:10.1161/01.cir.99.15.2027 · Cited by 676 · see citing works
Diet-induced atherosclerosis increases the release of nitrogen oxides from rabbit aorta.
Minor, R. L., Myers, P. R., Guerra, R., Bates, J. N., & Harrison, D. G. (1990) · Journal of Clinical Investigation · doi:10.1172/jci114949 · Cited by 517 · see citing works
Modified forms of low density lipoprotein and atherosclerosis
Aviram, M. (1993) · Atherosclerosis · doi:10.1016/0021-9150(93)90217-i · Cited by 345 · see citing works
Adams, V., Linke, A. H.-P., Kränkel, N., Erbs, S., Gielen, S., Möbius‐Winkler, S., Gummert, J. F., Mohr, F. W., Schuler, G. C., & Hambrecht, R. (2005) · Circulation · doi:10.1161/01.cir.0000154560.88933.7e · Cited by 337 · see citing works
Physical Inactivity Increases Oxidative Stress, Endothelial Dysfunction, and Atherosclerosis
Laufs, U., Wassmann, S., Czech, T., Münzel, T., Eisenhauer, M., Böhm, M., & Nickenig, G. (2005) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000158311.24443.af · Cited by 327 · see citing works
Social status, environment, and atherosclerosis in cynomolgus monkeys.
Kaplan, J. R., Manuck, S. B., Clarkson, T. B., Lusso, F. M., & Taub, D. M. (1982) · Arteriosclerosis: An Official Journal of the American Heart Association, Inc. · doi:10.1161/01.atv.2.5.359 · Cited by 320 · see citing works
Buja, L. M., Kita, T., Goldstein, J. L., Watanabe, Y., & Brown, M. S. (1983) · Arteriosclerosis An Official Journal of the American Heart Association Inc · doi:10.1161/01.atv.3.1.87 · Cited by 287 · see citing works
Black, P. H. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.04.008 · Cited by 276 · see citing works
Kaplan, J. R., Manuck, S. B., Adams, M. R., Weingand, K. W., & Clarkson, T. B. (1987) · Circulation · doi:10.1161/01.cir.76.6.1364 · Cited by 266 · see citing works
C-Reactive Protein, Inflammation, and Innate Immunity
Mortensen, R. F. (2001) · Immunologic Research · doi:10.1385/ir:24:2:163 · Cited by 238 · see citing works
Li, J., & Fang, C. (2004) · Medical Hypotheses · doi:10.1016/j.mehy.2003.12.014 · Cited by 228 · see citing works
The novel role of C-reactive protein in cardiovascular disease: Risk marker or pathogen
Wilson, A., Ryan, M. C., & Boyle, A. (2005) · International Journal of Cardiology · doi:10.1016/j.ijcard.2005.01.068 · Cited by 215 · see citing works
Cai, H. “., Li, Z., Dikalov, S., Holland, S. M., Hwang, J., Jo, H., Dudley, S. C., & Harrison, D. G. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m208884200 · Cited by 182 · see citing works
Catecholamine-Induced Vascular Wall Growth Is Dependent on Generation of Reactive Oxygen Species
Bleeke, T., Zhang, H., Madamanchi, N. R., Patterson, C., & Faber, J. E. (2003) · Circulation Research · doi:10.1161/01.res.0000109412.80157.7d · Cited by 162 · see citing works
Das, S., & O’Keefe, J. H. (2006) · Current Atherosclerosis Reports · doi:10.1007/s11883-006-0048-2 · Cited by 108 · see citing works
McCabe, P. M., Gonzales, J. A., Zaias, J., Szeto, A., Kumar, M., Herron, A. J., & Schneiderman, N. (2002) · Circulation · doi:10.1161/hc0302.102144 · Cited by 79 · see citing works
Self-citationLee, W., Allison, M., Kim, D., Song, C.-H., & Barrett-Connor, E. L. (2006) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2006.07.070 · Cited by 61 · see citing works
Claudio Napoli, A., Cicala, C., D’Armiento, F. P., Roviezzo, F., Somma, P., de Nigris, F., Zuliani, P., Bucci, M., Aleotti, L., Casini, A., et al. (1999) · General Pharmacology The Vascular System · doi:10.1016/s0306-3623(99)00043-9 · Cited by 41 · see citing works
Norepinephrine Stimulates Interleukin-6 mRNA Expression in Primary Cultured Rat Hepatocytes
Jung, B.-D., Kimura, E., Kitamura, H., et al. (2000) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a022596 · Cited by 35 · see citing works
Wolden‐Hanson, T., Davis, G. A., Baum, S. T., et al. (1993) · Obesity Research · doi:10.1002/j.1550-8528.1993.tb00003.x · Cited by 29 · see citing works
Social experience influences hypothalamic oxytocin in the WHHL rabbit
Paredes, J., Szeto, A., Levine, J. E., Zaias, J., Gonzales, J. A., Mendez, A. J., Llabre, M. M., Schneiderman, N., & McCabe, P. M. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.06.007 · Cited by 28 · see citing works
Self-citationGreco, A. M., Gambardella, P., Sticchi, R., et al. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90477-j · Cited by 16 · see citing works
Gonzales, J. A., Szeto, A., Mendez, A. J., Zaias, J., Paredes, J., Caperton, C. V., Llabre, M. M., Levine, J. E., Goldberg, R. B., Schneiderman, N., et al. (2005) · Psychosomatic Medicine · doi:10.1097/01.psy.0000155674.95497.ab · Cited by 8 · see citing works
Self-citation
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Perceived social isolation and cognition
Cacioppo, J. T., & Hawkley, L. C. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.06.005 · Cited by 2,144 · see citing works
Social relationships and health: The toxic effects of perceived social isolation
Cacioppo, J. T., & Cacioppo, S. (2014) · Social and Personality Psychology Compass · doi:10.1111/spc3.12087 · Cited by 1,057 · see citing works
Evolutionary mechanisms for loneliness
Cacioppo, J. T., Cacioppo, S., & Boomsma, D. I. (2014) · Cognition and Emotion · doi:10.1080/02699931.2013.837379 · Cited by 576 · see citing works
Cacioppo, J. T., Hawkley, L. C., Norman, G. J., & Berntson, G. G. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06028.x · Cited by 554 · see citing works
Modeling Social Influences on Human Health
Karelina, K., & DeVries, A. C. (2011) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3182002116 · Cited by 115 · see citing works
- Authors
- Nation, D. A., Gonzales, J. A., Mendez, A. J., Zaias, J., Szeto, A., Brooks, L. G., Paredes, J., D’Angola, A., Schneiderman, N., & McCabe, P. M.
- Affiliations
- University of Miami (US)
- Corresponding author
- McCabe, Philip M.
- Venue
- Psychosomatic Medicine
- Published
- 2008-04
- Volume
- 70
- Issue
- 3
- Pages
- 269-275
- ISSN
- 0033-3174 (ISSN-L)
- OpenAlex
- W1994386221
- Cited by
- 39
- References
- 27
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 5 · 2021: 1 · 2020: 3 · 2018: 3 · 2017: 2 · 2016: 1 · 2015: 1 · 2014: 1 · 2013: 3 · 2012: 3
- FWCI
- 1.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychosomatic Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (P01HL036588, HL36588, HL-04726)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Health and Mental Health
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Keywords
- social environment, atherosclerosis, oxidative stress, inflammation, Watanabe heritable hyperlipidemic rabbits, social isolation, physical inactivity, affiliative behavior, agonistic behavior, C-reactive protein, urinary catecholamines, NADPH oxidase, aortic arch, social stress
- MeSH terms
- Agonistic Behavior, Angiotensin II, Animals, Aorta, Thoracic, Arousal, C-Reactive Protein, Cholesterol, Epinephrine, Hyperlipidemias, Peptidyl-Dipeptidase A, Lipoproteins, HDL, Lipoproteins, LDL, Male, Norepinephrine, Rabbits, Social Environment, Social Isolation, Stress, Psychological, Reactive Oxygen Species, Oxidative Stress, Inflammation Mediators, NADPH Oxidases, Receptor, Angiotensin, Type 1, Atherosclerosis
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