Triactome: Neuro-immune-adipose interactions. Implication in vascular biology

Frontiers in Immunology

Volumn 5, Issue APR, 2014, Pages

  Chaldakov, George Nikov ^a   Fiore, Marco ^b   Ghenev, Peter I ^a   Beltowski, Jerzy ^c   Ranćić, Gorana ^d   Tunçel, Nese ^e   Aloe, Luigi ^b  

^a MEDICAL UNIVERSITY OF VARNA   (Bulgaria)

^b CNR   (Italy)

^c MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^d Medical Faculty University   (Serbia)

^e ESKISEHIR OSMANGAZI UNIVERSITY   (Turkey)

Author keywords

Adipokines; Adipose tissue; Atherosclerosis; BDNF; Lymphocytes; Mast cells; NGF; Perivascular nerves

Indexed keywords

NEUROTROPHIN; VASOCONSTRICTOR AGENT; VASODILATOR AGENT;

ADIPOSE TISSUE; ATHEROGENESIS; ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; BLOOD VESSEL WALL; CARDIOVASCULAR DISEASE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CYTOLOGY; HUMAN; HYPERTENSION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; METABOLIC DISORDER; MOLECULAR INTERACTION; NEUROIMMUNOLOGY; RESTENOSIS; REVIEW; TARGET CELL; TRIACTOME; VASCULAR BIOLOGY;

EID: 84900871821     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00130     Document Type: Review

References (121)

1. Soltis EE, Cassis LA. Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness. Clin Exp Hypertens (1991) A13:277-96.
2. Chaldakov GN, Fiore M, Ghenev PI, Stankulov IS, Aloe L. Atherosclerotic lesions: possible interactive involvement of intima, adventitia and associated adipose tissue. Int Med J (2000) 7:43-9.
3. Chaldakov GN, Fiore M, Ghenev PI, Stankulov IS, Angelucci F, Pavlov PS, et al. Conceptual novelties in atherogenesis: smooth muscle cells, adventitia, and adipose tissue. Biomed Rev (2000) 11:63-7. doi: 10.14748/bmr.v11.131.
4. Chaldakov GN, Stankulov IS, Aloe L. Subepicardial adipose tissue in human coronary atherosclerosis: another neglected phenomenon. Atherosclerosis (2001) 154:237-8. doi:10.1016/S0021-9150(00)00676-6.
5. Gollasch M, Dubrovska G. Paracrine role for periadventitial adipose tissue in the regulation of arterial tone. Trends Pharmacol Sci (2004) 25:647-53. doi:10.1016/j.tips.2004.10.005.
6. Yudkin JS, Eringa E, Stehouwer CDA. "Vasocrine" signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet (2005) 365:1817-20. doi:10.1016/S0140-6736(05)66585-3.
7. Chaldakov GN, Tonchev AB, Stankulov IS, Ghenev PI, Fiore M, Aloe L, et al. Periadventitial adipose tissue (tunica adiposa): enemy or friend around? Arch Pathol Lab Med (2007) 131:1766.
8. Verhagen SN, Buijsrogge MP, Vink A, van Herwerden LA, van der Graaf Y, Vissseren FL. Secretion of adipocytokines by perivascular adipose tissue near stenotic and non-stenotic coronary artery segments in patients undergoing CABG. Atherosclerosis (2014) 233:242-7. doi:10.1016/j.atherosclerosis.2013.12.005.
9. McKenney ML, Schultz KA, Boyd JH, Byrd JP, Alloosh M, Teague SD, et al. Epicardial adipose excision slows the progression of porcine coronary atherosclerosis. J Cardiothorac Surg (2014) 9:2-11. doi:10.1186/1749-8090-9-2.
10. Chaldakov GN, Tunçel N, Beltowski J, Fiore M, Ranćić G, Tonchev A, et al. Adipoparacrinology: an emerging field in biomedical research. Balkan Med J (2012) 29:2-9. doi:10.5152/balkanmedj.2012.022.
11. Bulloch JM, Daly CJ. Autonomic nerves and perivascular fat: interactive mechanisms. Pharmacol Ther (2014). doi:10.1016/j.pharmthera.2014.02.005.
12. Vaughan CH, Zarebidaki E, Ehlen JC, Bartness TJ. Analysis and measurement of the sympathetic and sensory innervation of white and brown adipose tissue. Methods Enzymol (2014) 537:199-225. doi:10.1016/B978-0-12-411619-1.00011-2.
13. Chaldakov GN, Vankov VN. Morphological aspects of secretion in the arterial smooth muscle cell, with special reference to the Golgi complex and microtubular cytoskeleton. Atherosclerosis (1986) 61:175-92. doi:10.1016/0021-9150(86)90137-1.
14. Chaldakov GN. Cardiovascular adipobiology: a novel. Heart-associated adipose tissue in cardiovascular disease. Ser J Exp Clin Res (2008) 9:81-8.
15. Ross R. Mechanisms of disease: atherosclerosis-an inflammatory disease. N Engl J Med (1999) 340:115-26. doi:10.1056/NEJM199901143400207.
16. Geng Y-J, Jonasson L. Linking immunity to atherosclerosis: implications for vascular pharmacology-a tribute to Göran K. Hansson. Vascul Pharmacol (2012) 56:29-33. doi:10.1016/j.vph.2011.11.001.
17. Inouye M, Silander K, Hamalainen E, Salomaa V, Harald K, Jousilahti P, et al. An immune response network associated with blood lipid levels. PLoS Genet (2010) 6:e1001113. doi:10.1371/journal.pgen.1001113.
18. Hilgendorf I, Theurl I, Gerhardt LM, Robbins CS, Weber GF, Gonen A, et al. Innate response activator B cells aggravate atherosclerosis by stimulating TH1 adaptive immunity. Circulation (2014). doi:10.1161/CIRCULATIONAHA.113.006381.
19. Tang YL, Yang YZ, Wang S, Huang T, Tang CK, Xu ZX, et al. Mast cell degranulator compound 48-80 promotes atherosclerotic plaque in apolipoprotein E knockout mice with perivascular common carotid collar placement. Chin Med J (2009) 122:319-25.
20. Booth RFC, Martin JF, Honey AC, Hassall DG, Beesley JE, Moncada S. Rapid development of atherosclerotic lesions in the rabbit carotid artery induced by perivascular manipulation. Atherosclerosis (1989) 76:257-68. doi:10.1016/0021-9150(89)90109-3.
21. Scott TM, Honey AC, Martin JF, Booth RF. Perivascular innervation is lost in experimental atherosclerosis. Cardioscience (1992) 3:145-53.
22. Laine P, Naukkarinen A, Heikkila L, Penttila A, Kovanen PT. Adventitial mast cells connect with sensory nerve fibers in atherosclerotic coronary arteries. Circulation (2000) 101:1665-9. doi:10.1161/01.CIR.101.14.1665.
23. Bot I, de Jager SC, Bot M, van Heiningen SH, de Groot P, Veldhuizen RW, et al. The neuropeptide substance P mediates adventitial mast cell activation and induces intraplaque hemorrhage in advanced atherosclerosis. Circ Res (2010) 106:89-92. doi:10.1161/CIRCRESAHA.109.204875.
24. Levi-Montalcini R. The nerve growth factors 35 years later. Science (1987) 237:1154-62. doi:10.1126/science.3306916.
25. Chaldakov GN, Ghenev PI, Andonov M, Valchanov K, Tonchev A, Pancheva R. Neural-immune-effector (NIE) cross-talk in vascular trophobiology: proposal for new and not yet exploited purinergic regulatory mechanisms. Biomed Rev (1994) 3:81-6. doi:10.14748/bmr.v3.205.
26. Chaldakov G. Neural-immune-effector trophic interaction: an emerging concept for the neurotrophic theory [abstract]. Folia Anat (1996) 24(Suppl 2):24.
27. Azoulay D, Urshansky N, Karni A. Low and dysregulated BDNF secretion from immune cells of MS patients is related to reduced neuroprotection. J Neuroimmunol (2008) 195:186-93. doi:10.1016/j.jneuroim.2008.01.010.
28. Fiore M, Chaldakov GN, Aloe L. Nerve growth factor as a signaling molecule for nerve cells and also for the neuroendocrine-immune systems. Rev Neurosci (2009) 20:133-45. doi:10.1515/REVNEURO.2009.20.2.133.
29. Aloe L, Levi-Montalcini R. Mast cells increase in tissues of neonatal rats injected with the nerve growth factor. Brain Res (1977) 133:358-66. doi:10.1016/0006-8993(77)90772-7.
30. Hasan W, Jama A, Donohue T, Wernli G, Onyszchuk G, Al-Hafez B, et al. Sympathetic hyperinnervation and inflammatory cell NGF synthesis following myocardial infarction in rats. Brain Res (2006) 1124:142-54. doi:10.1016/j.brainres.2006.09.054.
31. Bracci-Laudiero L, Aloe L, Caroleao MC, Buanne P, Costa N, Starace G, et al. Endogenous NGF regulates CGRP expression in human monocytes, and affects HLA-DR and CD86 expression and IL-10 production. Blood (2005) 106:3507-14. doi:10.1182/blood-2004-10-4055.
32. Leon A, Buriani A, Dal Toso R, Fabris M, Romanello S, Aloe L, et al. Mast cells synthesize, store, and release nerve growth factor. Proc Natl Acad Sci U S A (1994) 91:3739-43. doi:10.1073/pnas.91.9.3739.
33. Wernli G, Hasan W, Bhattacherjee A, van Rooijen N, Smith PG. Macrophage depletion suppresses sympathetic hyperinnervation following myocardial infarction. Basic Res Cardiol (2009) 104:681-93. doi:10.1007/s00395-009-0033-3.
34. Chaldakov GN, Fiore M, Stankulov IS, Manni L, Hristova MG, Antonelli A, et al. Neurotrophin presence in human coronary atherosclerosis and metabolic syndrome: a role for NGF and BDNF in cardiovascular disease? Prog Brain Res (2004) 146:279-89. doi:10.1016/S0079-6123(03)46018-4.
35. Chaldakov GN, Fiore M, Stankulov IS, Hristova M, Antonelli A, Manni L, et al. NGF, BDNF, leptin, and mast cells in human coronary atherosclerosis and metabolic syndrome. Arch Physiol Biochem (2001) 109:357-60. doi:10.1076/apab.109.3.357.9353.
36. Navarro-Tableros V, Fiordelisio T, Hernandez-Cruz A, Hiriart M. Nerve growth factor promotes development of glucose-induced insulin secretion in rat neonate pancreatic beta cells by modulating calcium channels. Channels (Austin) (2007) 1:408-16. doi:10.4161/chan.1.6.5450.
37. Cuzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med (2007) 204:2449-60. doi:10.1084/jem.20070657.
38. de Kloet AD, Krause EG, Shi PD, Zubcevic J, Raizada MK, Sumners C. Neuroimmune communication in hypertension and obesity: a new therapeutic angle? Pharmacol Ther (2013) 138:428-40. doi:10.1016/j.pharmthera.2013.02.005.
39. Kasselman LJ, Sideris A, Bruno C, Perez WR, Cai N, Nicoletti JN, et al. BDNF: a missing link between sympathetic dysfunction and inflammatory disease? J Neuroimmunol (2006) 175:118-27. doi:10.1016/j.jneuroim.2006.03.008.
40. Divoux A, Moutel S, Poitou C, Lacasa D, Veyrie N, Aissat A, et al. Mast cells in human adipose tissue: link with morbid obesity, inflammatory status, and diabetes. J Clin Endocrinol Metab (2012) 97:E1677-85. doi:10.1210/jc.2012-1532.
41. Pucino V, De Rosa V, Procaccini C, Matarese G. Regulatory T cells, leptin and angiogenesis. Chem Immunol Allergy (2014) 99:155-69. doi:10.1159/000353557.
42. Jin C, Flavell RA. Innate sensors of pathogen and stress: linking inflammation to obesity. J Allergy Clin Immunol (2013) 132:287-94. doi:10.1016/j.jaci.2013.06.022.
43. Winer DA, Winer S, Chang MH, Shen L, Engleman EGB. Lymphocytes in obesity-related adipose tissue inflammation and insulin resistance. Cell Mol Life Sci (2014) 71:1033-43. doi:10.1007/s00018-013-1486-y.
44. O'Rourke RW, Gaston GD, Meyer KA, White AE, Marks DL. Adipose tissue NK cells manifest an activated phenotype in human obesity. Metabolism (2013) 62:1557-61. doi:10.1016/j.metabol.2013.07.011.
45. Makki K, Froguel P, Wolowczuk I. Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines. ISRN Inflamm (2013) 2013:139239. doi:10.1155/2013/139239.
46. Boumié A, Casteilla L, Lafontan M. Adipose tissue lymphocytes and macrophages in obesity and insulin resistance: makers or markers, and which comes first? Arterioscler Thromb Vasc Biol (2008) 28:1211-3. doi:10.1161/ATVBAHA.108.168229.
47. Priceman SJ, Kujawski M, Shen S, Cherryholmes GA, Lee H, Zhang C, et al. Regulation of adipose tissue T cell subsets by Stat3 is crucial for diet-induced obesity and insulin resistance. Proc Natl Acad Sci U S A (2013) 110:13079-84. doi:10.1073/pnas.1311557110.
48. Vyas H, Krishnaswamy G. Paul Ehrlich's "Mastzellen"-from aniline dyes to DNA chip arrays: a historical review of developments in mast cell research. Methods Mol Biol (2006) 315:3-11.
49. Bot I, Biessen EAL. Mast cells in atherosclerosis. Thromb Haemost (2011) 106:820-6. doi:10.1160/TH11-05-0291.
50. Lee BC, Lee J. Cellular and molecular players in adipose tissue inflammation in the development of obesity-induced insulin resistance. Biochim Biophys Acta (2014) 1842:446-62. doi:10.1016/j.bbadis.2013.05.017.
51. Shi MA, Shi GP. Different roles of mast cells in obesity and diabetes: lessons from experimental animals and humans. Front Immunol (2012) 25(3):7. doi:10.3389/fimmu.2012.00007.
52. Galli SJ, Tsai M. Mast cells: versatile regulators of inflammation, tissue remodeling, host defense and homeostasis. J Dermatol Sci (2008) 49:7-19. doi:10.1016/j.jdermsci.2007.09.009.
53. Zhang J, Shi G-P. Masts cells and metabolic syndrome. Biochim Biophys Acta (2012) 1822:14-20. doi:10.1016/j.bbadis.2010.12.012.
54. Altintas MM, Nayer B, Walford EC, Johnson KB, Gaidosh G, Reiser J, et al. Leptin deficiency-induced obesity affects the density of mast cells in abdominal fat depots and lymph nodes in mice. Lipids Health Dis (2012) 11:21. doi:10.1186/1476-511X-11-21.
55. Pond CM. Adipose tissue and the immune system. Prostaglandins Leukot Essent Fatty Acids (2005) 73:17-30. doi:10.1016/j.plefa.2005.04.005.
56. Wilcox JN, Scott NA. Potential role of the adventitia in arteritis and atherosclerosis. Int J Cardiol (1996) 54(Suppl):S21-35. doi:10.1016/S0167-5273(96)02811-2.
57. Shi Y, O'Brien JE, Fard A, Mannion JD, Wang D, Zalewski A. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation (1996) 94:1655-64. doi:10.1161/01.CIR.94.7.1655.
58. Ghenev PI, Chaldakov GN. Neural-immune links in adventitial remodeling in human coronary atherosclerosis. Circulation (1997) 96:2083-4.
59. Huehns TY, Gonschior P, Hofling B. Adventitia as a target for intravascular local drug delivery. Heart (1996) 75:537-8. doi:10.1136/hrt.75.6.537.
60. Chaldakov GN, Stankulov IS, Fiore M, Ghenev PI, Aloe L. Nerve growth factor levels and mast cell distribution in human coronary atherosclerosis. Atherosclerosis (2001) 159:57-66. doi:10.1016/S0021-9150(01)00488-9.
61. Hasan W, Smith PG. Decreased adrenoceptor stimulation in heart failure rats reduces NGF expression by cardiac parasympathetic neurons. Auton Neurosci (2014) 181:13-20. doi:10.1016/j.autneu.2013.11.001.
62. Romo-Yáñez J, Velasco M, Larqué C, Chávez-Maldonado JP, Hiriart M. Differential expression of NGF and BDNF in rat adipose depots during early development and adulthood. Adipobiology (2013) 5:39-43.
63. Aloe L, Tirassa P, Lambiase A. The topical application of nerve growth factor as a pharmacological tool for human corneal and skin ulcers. Pharmacol Res (2008) 57:253-8. doi:10.1016/j.phrs.2008.01.010.
64. Hotamisligil GS. Inflammation and metabolic disorders. Nature (2006) 444:860-7. doi:10.1038/nature05485.
65. Dali-Youcef N, Mecili M, Ricci R, Andrès E. Metabolic inflammation: connecting obesity and insulin resistance. Ann Med (2013) 45:242-53. doi:10.3109/07853890.2012.705015.
66. Chaldakov GN, Stankulov IS, Hristova M, Ghenev PI. Adipobiology of disease: adipokines and adipokine-targeted pharmacology. Curr Pharm Des (2003) 9:1023-31. doi:10.2174/1381612033455152.
67. Louise TE, Saeed N, Hajnal JV, Brynes A, Goldstone AP, Frost G, et al. Magnetic resonance imaging of total body fat. J Appl Physiol (1998) 85:1778-85.
68. Chaldakov GN, Fiore M, Tonchev AB, Dimitrov D, Pancheva R, Ranćić G, et al. Homo obesus: a metabotrophin-deficient species. Pharmacology and nutrition insight. Curr Pharm Des (2007) 13:2176-9. doi:10.2174/138161207781039616.
69. Aloe L, Tonchev AB, Fiore M, Chaldakov GN. Homo diabesus: involvement of metabotrophic factors. Adipobiology (2013) 5:45-9.
70. Sacks H, Symonds ME. Anatomical locations of human brown adipose tissue functional relevance and implications in obesity and type 2 diabetes. Diabetes (2013) 62:1783-90. doi:10.2337/db12-1430.
71. Chechi K, Nedergaard J, Richard D. Brown adipose tissue as an anti-obesity tissue in humans. Obes Rev (2014) 15:92-106. doi:10.1111/obr.12116.
72. Giralt M, Villarrova F. White, brown, beige/brite: different adipose cells for different functions? Endocrinology (2013) 154:2992-3000. doi:10.1210/en.2013-1403.
73. Marchington JM, Mattacks CA, Pond CM. Adipose tissue in the mammalian heart and pericardium: structure, foetal development and biochemical properties. Comp Biochem Physiol B (1989) 94:225-32.
74. Poursharifi P, Lapointe M, Pétrin D, Devost D, Gauvreau D, Hébert TE, et al. C5L2 and C5aR interaction in adipocytes and macrophages: insights into adipoimmunology. Cell Signal (2013) 25:910-9. doi:10.1016/j.cellsig.2012.12.010.
75. Chaldakov GN, Fiore M, Tonchev AB, Aloe L. Neuroadipology: a novel component of neuroendocrinology. Cell Biol Int (2010) 34:1051-3. doi:10.1042/CBI20100509.
76. Renes J, Mariman E. Application of proteomics technology in adipocyte biology. Mol Biosyst (2013) 9:1076-91. doi:10.1039/c3mb25596d.
77. Hausman GJ, Barb CR, Dean RG. Patterns of gene expression in pig adipose tissue: insulin-like growth factor system proteins, neuropeptide Y (NPY), NPY receptors, neurotrophic factors and other secreted factors. Domest Anim Endocrinol (2008) 35:24-34. doi:10.1016/j.domaniend.2008.01.004.
78. Sornelli F, Fiore M, Chaldakov GN, Aloe L. Adipose tissue-derived nerve growth factor and brain-derived neurotrophic factor: results from experimental stress and diabetes. Gen Physiol Biophys (2009) 28:179-83.
79. Ryan VH, German AJ, Wood IS, Hunter L, Morris P, Trayhurn P. NGF gene expression and secretion by canine adipocytes in primary culture: upregulation by the inflammatory mediators LPS and TNFalpha. Horm Metab Res (2008) 40:861-8. doi:10.1055/s-0028-1083782.
80. Trayhurn P, de Heredia FP, Wang B, de Oliveira C, González-Muniesa P, Wood SI. Cellular hypoxia: a key modulator of adipocyte function in obesity? Adipobiology (2009) 1:19-26. doi:10.1038/ijo.2011.279.
81. Takaoka M, Nagata D, Kihara S, Shimomura I, Kimura Y, Tabata Y, et al. Periadventitial adipose tissue plays a critical role in vascular remodeling. Circ Res (2009) 105:906-11. doi:10.1161/CIRCRESAHA.109.199653.
82. Nakamura K, Fuster JJ, Walsh K. Adipokines: a link between obesity and cardiovascular disease. J Cardiol (2013). doi:10.1016/j.jjcc.2013.11.006.
83. Almabrouk TA, Ewart MA, Salt IP, Kennedy S. Perivascular fat, AMP-activated protein kinase and vascular diseases. Br J Pharmacol (2014) 171:595-617. doi:10.1111/bph.12479.
84. Brandes RP. The fatter the better? Perivascular adipose tissue attenuates vascular contraction through different mechanisms. Br J Pharmacol (2007) 151:303-4. doi:10.1038/sj.bjp.0707229.
85. Spiroglou SG, Kostopoulos CG, Varakis JN, Papadaki HH. Adipokines in periaortic and epicardial adipose tissue: differential expression and relation to atherosclerosis. J Atheroscler Thromb (2010) 17:115-30. doi:10.5551/jat.1735.
86. Rossi C, Santini E, Chiarugi M, Salvati A, Comassi M, Vitolo E, et al. The complex P2X7 receptor/inflammasome in perivascular fat tissue of heavy smokers. Eur J Clin Invest (2014) 44:295-302. doi:10.1111/eci.12232.
87. Lu C, Su LY, Lee RM, Gao YJ. Mechanisms for perivascular adipose tissue-mediated potentiation of vascular contraction to perivascular neuronal stimulation: the role of adipocyte-derived angiotensin II. Eur J Pharmacol (2010) 634:107-12. doi:10.1016/j.ejphar.2010.02.006.
88. Yanev S, Aloe L, Fiore F, Chaldakov GN. Neurotrophic and metabotrophic potential of nerve growth factor and brain-derived neurotrophic factor: linking cardiometabolic and neuropsychiatric diseases. World J Pharmacol (2013) 2:92-9. doi:10.5497/wjp.v2.i4.92.
89. Hoang PT, Park P, Cobb LJ, Paharkova-Vatchkova V, Hakimi M, Cohen P, et al. The neurosurvival factor Humanin inhibits beta-cell apoptosis via signal transducer and activator of transcription 3 activation and delays and ameliorates diabetes in nonobese diabetic mice. Metabolism (2010) 59:343-9. doi:10.1016/j.metabol.2009.08.001.
90. Tack CJ, Stienstra R, Joosten LA, Netea MG. Inflammation links excess fat to insulin resistance: the role of the interleukin-1 family. Immunol Rev (2012) 249:239-52. doi:10.1111/j.1600-065X.2012.01145.x.
91. Gomez-Pinilla F, Vaynman S, Ying Z. Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur J Neurosci (2008) 28:2278-87. doi:10.1111/j.1460-9568.2008.06524.x.
92. Cushing P, Bhalla R, Johnson AM, Rushlow WJ, Meakin SO, Belliveau DJ. Nerve growth factor increases connexin43 phosphorylation and gap junctional intercellular communication. J Neurosci Res (2005) 82:788-801. doi:10.1002/jnr.20689.
93. Becker DL, Thrasivoulou C, Phillips AR. Connexins in wound healing; perspectives in diabetic patients. Biochim Biophys Acta (2012) 1818:2068-75. doi:10.1016/j.bbamem.2011.11.017.
94. Novelle MG, Contreras C, Romero-Picó A, López M, Diéguez C. Irisin, two years later. Int J Endocrinol (2013) 2013:746281. doi:10.1155/2013/746281.
95. Iacobellis G, Di Gioia C, Petramala L, Chiappetta C, Serra V, Zinnamosca L, et al. Brown fat expresses adiponectin in humans. Int J Endocrinol (2013) 2013:126751. doi:10.1155/2013/126751.
96. Tan BK, Adya R, Randeva HS. Omentin: a novel link between inflammation, diabesity, and cardiovascular disease. Trends Cardiovasc Med (2010) 20:143-8. doi:10.1016/j.tcm.2010.12.002.
97. Castan-Laurell I, Dray C, Attané C, Duparc T, Knauf C, Valet P. Apelin, diabetes, and obesity. Endocrine (2011) 40:1-9. doi:10.1007/s12020-011-9507-9.
98. Wang GX, Cho KW, Uhm M, Hu CR, Li S, Cozacov Z, et al. Otopetrin 1 protects mice from obesity-associated metabolic dysfunction through attenuating adipose tissue inflammation. Diabetes (2013). doi:10.2337/db13-1139.
99. Hellmann J, Tang Y, Kosuri M, Bhatnagar A, Spite M. Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice. FASEB J (2011) 25:2399-407. doi:10.1096/fj.10-178657.
100. Benomar Y, Gertler A, De Lacy P, Crépin D, Ould Hamouda H, Riffault L, et al. Central resistin overexpression induces insulin resistance through toll-like receptor 4. Diabetes (2013) 62:102-14. doi:10.2337/db12-0237.
101. Govoni S, Pascale A, Amadio M, Calvillo L, D'Elia E, Cereda C, et al. NGF and heart: is there a role in heart disease? Pharmacol Res (2011) 63:266-77. doi:10.1016/j.phrs.2010.12.017.
102. Asanome A, Kawabe J, Matsuki M, Kabara M, Hira Y, Bochimoto H, et al. Nerve growth factor stimulates regeneration of perivascular nerve, and induces the maturation of microvessels around the injured artery. Biochem Biophys Res Commun (2014) 443:150-5. doi:10.1016/j.bbrc.2013.11.070.
103. Prencipe G, Minnone G, Strippoli R, De Pasquale L, Petrini S, Caiello I, et al. Nerve growth factor downregulates inflammatory response in human monocytes through TrkA. J Immunol (2014). doi:10.4049/jimmunol.1300825.
104. Fruhbeck G, Becerril S, Sáinz N, Garrastachu P, Garcia-Velloso MJ. BAT: a new target for human obesity. Trends Pharmacol Sci (2009) 30:387-96. doi:10.1016/j.tips.2009.05.003.
105. Poursharifi P, Rezvani R, Gupta A, Lapointe M, Marceau P, Tchernof A, et al. Association of immune and metabolic receptors C5aR and C5L2 with adiposity in women. Mediators Inflamm (2014) 2014:413921. doi:10.1155/2014/413921.
106. Ramkhelawon B, Hennessy EJ, Ménager M, Ray TD, Sheedy FJ, Hutchison S. Netrin-1 promotes adipose tissue macrophage retention and insulin resistance in obesity. Nat Med (2014). doi:10.1038/nm.3467.
107. Bongo JB, Peng DQ. The neuroimmune guidance cue netrin-1: a new therapeutic target in cardiovascular disease. J Cardiol (2014) 63:95-8. doi:10.1016/j.jjcc.2013.10.006.
108. Pae M, Romeo GR. The multifaceted role of profilin-1 in adipose tissue inflammation and glucose homeostasis. Adipocyte (2014) 3:69-74. doi:10.4161/adip.26965.
109. Dashwood MR, Dooley A, Shi-Wen X, Abraham DJ, Souza DS. Does periadventitial fat-derived nitric oxide play a role in improved saphenous vein graft patency in patients undergoing coronary artery bypass surgery? J Vasc Res (2007) 44:175-81. doi:10.1159/000099833.
110. Malinowski M, Deja MA, Golba KS, Roleder T, Biernat J, Wos S. Perivascular tissue of internal thoracic artery releases potent nitric oxide and prostacyclin-independent anticontractile factor. Eur J Cardiothorac Surg (2008) 33:225-31. doi:10.1016/j.ejcts.2007.11.007.
111. Fesüs G, Dubrovska G, Gorzelniak K, Kluge R, Huang Y, Luft FC, et al. Adiponectin is a novel humoral vasodilator. Cardiovasc Res (2007) 75:719-27. doi:10.1016/j.cardiores.2007.05.025.
112. Gao YJ, Takemori K, Su LY, An WS, Lu C, Sharma AM, et al. Perivascular adipose tissue promotes vasoconstriction: the role of superoxide anion. Cardiovasc Res (2006) 71:363-73. doi:10.1016/j.cardiores.2006.03.013.
113. Tunçel N, Peker E, Sener E, Dal AG, Tunçel M, Chaldakov GN, et al. Cold exposure and adipose nitric oxide and mast cells: influence on aorta contractility. Adipobiology (2009) 1:67-75. doi:10.14748/adipo.v1.251.
114. Wojcicka G, Jamroz-Wisniewska A, Attanasova P, Chaldakov GN, Chylinska-Kula B, Beltowski J. Differential effects of statins on endogenous H2S formation in perivascular adipose tissue. Pharmacol Res (2011) 63:68-76. doi:10.1016/j.phrs.2010.10.011.
115. Yamawaki H, Hara N, Okada M, Hara Y. Visfatin causes endothelium-dependent relaxation in isolated blood vessels. Biochem Biophyis Res Commun (2009) 383:503-8. doi:10.1016/j.bbrc.2009.04.074.
116. Miao CY, Li ZY. The role of perivascular adipose tissue in vascular smooth muscle cell growth. Br J Pharmacol (2012) 165:643-58. doi:10.1111/j.1476-5381.2011.01404.x.
117. Yamawaki H, Tsubaki N, Mukohda M, Okada M, Hara Y. Omentin, a novel adipokine, induces vasodilation in rat isolated blood vessels. Biochem Biophyis Res Commun (2010) 393:668-72. doi:10.1016/j.bbrc.2010.02.053.
118. Oriowo MA. Perivascular adipose tissue, vascular reactivity and hypertension. Med Princ Pract (2014). doi:10.1159/000356380.
119. Sacks HS. Weight loss in obesity reduces epicardial fat thickness; so what? J Appl Physiol (2009) 106:1-2. doi:10.1152/japplphysiol.91396.2008.
120. Skilton MR, Sérusclat A, Sethu AH, Brun S, Bernard S, Balkau B, et al. Noninvasive measurement of carotid extra-media thickness: associations with cardiovascular risk factors and intima-media thickness. JACC Cardiovasc Imaging (2009) 2:176-82. doi:10.1016/j.jcmg.2008.09.013.
121. Schlett CL, Hoffmann U. Identification and quantification of fat compartments with CT and MRI and their importance. Radiologe (2011) 51:372-8. doi:10.1007/s00117-010-2088-4.