Toll-like receptors 2 and 4 modulate autonomic control of heart rate and energy metabolism

Brain, Behavior, and Immunity

Volumn 36, Issue , 2014, Pages 90-100

  Okun, Eitan ^a   Griffioen, Kathleen J ^b   Rothman, Sarah ^b   Wan, Ruiqian ^b   Cong, Wei Na ^c   De Cabo, Rafael ^c   Martin Montalvo, Alejandro ^c   Levette, Andrew ^c   Maudsley, Stuart ^b   Martin, Bronwen ^c   Arumugam, Thiruma Valavan ^d   Mattson, Mark P ^b,e  

^a BAR ILAN UNIVERSITY   (Israel)

^b Departments of Neuroscience   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ANS; Autonomic nervous system; Heart rate; Innate immunity; Stress; TLR2; TLR4; Toll like receptors

Indexed keywords

TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BASAL BODY TEMPERATURE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; ENERGY METABOLISM; FOOD INTAKE; HEART RATE; IMMOBILIZATION STRESS; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PARASYMPATHETIC TONE; PRIORITY JOURNAL; THERMOREGULATION; WILD TYPE; YOUNG ADULT;

ANS; AUTONOMIC NERVOUS SYSTEM; HEART RATE; INNATE IMMUNITY; STRESS; TLR2; TLR4; TOLL-LIKE RECEPTORS;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; BODY TEMPERATURE; BODY TEMPERATURE REGULATION; ENERGY METABOLISM; HEART RATE; MALE; MICE; MICE, KNOCKOUT; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84891834946     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.10.013     Document Type: Article

References (59)

1. Akira S. Mammalian toll-like receptors. Curr. Opin. Immunol. 2003, 15:5-11.
2. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by toll-like receptor 3. Nature 2001, 413:732-738.
3. Anker S.D., von Haehling S. Inflammatory mediators in chronic heart failure: an overview. Heart 2004, 90:464-470.
4. Bartness T.J., Vaughan C.H., Song C.K. Sympathetic and sensory innervation of brown adipose tissue. Int. J. Obes. (London) 2010, 34(Suppl 1):S36-S42.
5. Bexis S., Docherty J.R. Role of alpha 1- and beta 3-adrenoceptors in the modulation by SR59230A of the effects of MDMA on body temperature in the mouse. British J. Pharmacol. 2009, 158:259-266.
6. Bigger J.T., Fleiss J.L., Steinman R.C., Rolnitzky L.M., Kleiger R.E., Rottman J.N. Frequency domain measures of heart period variability and mortality after myocardial infarction. Circulation 1992, 85:164-171.
7. Birks E.J., Felkin L.E., Banner N.R., Khaghani A., Barton P.J., Yacoub M.H. Increased toll-like receptor 4 in the myocardium of patients requiring left ventricular assist devices. J. Heart Lung Transplant.: Offic. Public. Int. Soc. Heart Transplantat. 2004, 23:228-235.
8. Bomfim G.F., Dos Santos R.A., Oliveira M.A., Giachini F.R., Akamine E.H., Tostes R.C., Fortes Z.B., Webb R.C., Carvalho M.H. Toll-like receptor 4 contributes to blood pressure regulation and vascular contraction in spontaneously hypertensive rats. Clin. Sci. (London) 2012, 122:535-543.
9. Brown R.D., Ambler S.K., Mitchell M.D., Long C.S. The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Ann. Rev. Pharmacol. Toxicol. 2005, 45:657-687.
10. Bsibsi M., Ravid R., Gveric D., van Noort J.M. Broad expression of toll-like receptors in the human central nervous system. J. Neuropathol. Exp. Neurol. 2002, 61:1013-1021.
11. Cameron J.S., Alexopoulou L., Sloane J.A., DiBernardo A.B., Ma Y., Kosaras B., Flavell R., Strittmatter S.M., Volpe J., Sidman R., Vartanian T. Toll-like receptor 3 is a potent negative regulator of axonal growth in mammals. J. Neurosci. 2007, 27:13033-13041.
12. Cannon B., Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 2004, 84:277-359.
13. Caricilli A.M., Picardi P.K., de Abreu L.L., Ueno M., Prada P.O., Ropelle E.R., Hirabara S.M., Castoldi A., Vieira P., Camara N.O., Curi R., Carvalheira J.B., Saad M.J. Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice. PLoS Biol. 2011, 9:e1001212.
14. Chartoumpekis D.V., Habeos I.G., Ziros P.G., Psyrogiannis A.I., Kyriazopoulou V.E., Papavassiliou A.G. Brown adipose tissue responds to cold and adrenergic stimulation by induction of FGF21. Mol. Med. 2011, 17:736-740.
15. Ehrentraut H., Weber C., Ehrentraut S., Schwederski M., Boehm O., Knuefermann P., Meyer R., Baumgarten G. The toll-like receptor 4-antagonist eritoran reduces murine cardiac hypertrophy. European J. Heart Fail. 2011, 13:602-610.
16. Ehrentraut S., Lohner R., Schwederski M., Ehrentraut H., Boehm O., Noga S., Langhoff P., Baumgarten G., Meyer R., Knuefermann P. In vivo toll-like receptor 4 antagonism restores cardiac function during endotoxemia. Shock 2011, 36:613-620.
17. Eichhorn E.J., Bristow M.R. Medical therapy can improve the biological properties of the chronically failing heart. A new era in the treatment of heart failure. Circulation 1996, 94:2285-2296.
18. Favre J., Musette P., Douin-Echinard V., Laude K., Henry J.P., Arnal J.F., Thuillez C., Richard V. Toll-like receptors 2-deficient mice are protected against postischemic coronary endothelial dysfunction. Arteriosclerosis, Thrombosis, Vascular Biology 2007, 27:1064-1071.
19. Foldes G., von Haehling S., Okonko D.O., Jankowska E.A., Poole-Wilson P.A., Anker S.D. Fluvastatin reduces increased blood monocyte toll-like receptor 4 expression in whole blood from patients with chronic heart failure. Int. J. Cardiol. 2008, 124:80-85.
20. Francis G.S. The relationship of the sympathetic nervous system and the renin-angiotensin system in congestive heart failure. Am. Heart J. 1989, 118:642-648.
21. Frantz S., Kobzik L., Kim Y.D., Fukazawa R., Medzhitov R., Lee R.T., Kelly R.A. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J. Clin. Invest. 1999, 104:271-280.
22. Fu L., Isobe K., Zeng Q., Suzukawa K., Takekoshi K., Kawakami Y. The effects of beta(3)-adrenoceptor agonist CL-316,243 on adiponectin, adiponectin receptors and tumor necrosis factor-alpha expressions in adipose tissues of obese diabetic KKAy mice. European J. Pharmacol. 2008, 584:202-206.
23. Garrafa E., Imberti L., Tiberio G., Prandini A., Giulini S.M., Caimi L. Heterogeneous expression of toll-like receptors in lymphatic endothelial cells derived from different tissues. Immunol. Cell Biol. 2011, 89:475-481.
24. Goldsmith S.R. Angiotensin II and sympathoactivation in heart failure. J. Card Fail. 1999, 5:139-145.
25. Gradman A.H., Alfayoumi F. From left ventricular hypertrophy to congestive heart failure: management of hypertensive heart disease. Prog. Cardiovasc. Dis. 2006, 48:326-341.
26. Griffioen K.J., Wan R., Okun E., Wang X., Lovett-Barr M.R., Li Y., Mughal M.R., Mendelowitz D., Mattson M.P. GLP-1 receptor stimulation depresses heart rate variability and inhibits neurotransmission to cardiac vagal neurons. Cardiovasc. Res. 2011, 89:72-78.
27. Griffioen K.J., Rothman S.M., Ladenheim B., Wan R., Vranis N., Hutchison E., Okun E., Cadet J.L., Mattson M.P. Dietary energy intake modifies brainstem autonomic dysfunction caused by mutant alpha-synuclein. Neurobiol. Aging 2013, 34:928-935.
28. Ha T., Li Y., Hua F., Ma J., Gao X., Kelley J., Zhao A., Haddad G.E., Williams D.L., William Browder I., Kao R.L., Li C. Reduced cardiac hypertrophy in toll-like receptor 4-deficient mice following pressure overload. Cardiovasc. Res. 2005, 68:224-234.
29. Hofmann U., Ertl G., Frantz S. Toll-like receptors as potential therapeutic targets in cardiac dysfunction. Exp. Opin. Therapeutic Targets 2011, 15:753-765.
30. Hubschle T., Mutze J., Muhlradt P.F., Korte S., Gerstberger R., Roth J. Pyrexia, anorexia, adipsia, and depressed motor activity in rats during systemic inflammation induced by the toll-like receptors-2 and -6 agonists MALP-2 and FSL-1. American journal of physiology. Regulatory, Integrative Comparative Physiology 2006, 290:R180-R187.
31. Lathia J.D., Okun E., Tang S.C., Griffioen K., Cheng A., Mughal M.R., Laryea G., Selvaraj P.K., ffrench-Constant C., Magnus T., Arumugam T.V., Mattson M.P. Toll-like receptor 3 is a negative regulator of embryonic neural progenitor cell proliferation. J. Neurosci. 2008, 28:13978-13984.
32. Ma Y., Li J., Chiu I., Wang Y., Sloane J.A., Lu J., Kosaras B., Sidman R.L., Volpe J.J., Vartanian T. Toll-like receptor 8 functions as a negative regulator of neurite outgrowth and inducer of neuronal apoptosis. J. Cell Biol. 2006, 175:209-215.
33. Ma Y., Haynes R.L., Sidman R.L., Vartanian T. TLR8: an innate immune receptor in brain, neurons and axons. Cell Cycle 2007, 6:2859-2868.
34. Marques R., Boneca I.G. Expression and functional importance of innate immune receptors by intestinal epithelial cells. Cell. Mol. life Sci.: CMLS 2011, 68:3661-3673.
35. Meredith I.T., Eisenhofer G., Lambert G.W., Dewar E.M., Jennings G.L., Esler M.D. Cardiac sympathetic nervous activity in congestive heart failure. Evidence for increased neuronal norepinephrine release and preserved neuronal uptake. Circulation 1993, 88:136-145.
36. Mersmann J., Berkels R., Zacharowski P., Tran N., Koch A., Iekushi K., Dimmeler S., Granja T.F., Boehm O., Claycomb W.C., Zacharowski K. Preconditioning by toll-like receptor 2 agonist Pam3CSK4 reduces CXCL1-dependent leukocyte recruitment in murine myocardial ischemia/reperfusion injury. Crit. Care Med. 2010, 38:903-909.
37. Nakagawa Y., Maeda H., Murai T. Evaluation of the in vitro pyrogen test system based on proinflammatory cytokine release from human monocytes: comparison with a human whole blood culture test system and with the rabbit pyrogen test. Clin. Diag. Lab. Immunol. 2002, 9:588-597.
38. Navi A., Patel H., Shaw S., Baker D., Tsui J. Therapeutic role of toll-like receptor modification in cardiovascular dysfunction. Vasc. Pharmacol. 2013, 58:231-239.
39. Ogawa K., Hirooka Y., Kishi T., Sunagawa K. Brain AT1 receptor activates the sympathetic nervous system through toll-like receptor 4 in mice with heart failure. J. Cardiovasc. Pharmacol. 2011, 58:543-549.
40. Okun E., Griffioen K., Barak B., Roberts N.J., Castro K., Pita M.A., Cheng A., Mughal M.R., Wan R., Ashery U., Mattson M.P. Toll-like receptor 3 inhibits memory retention and constrains adult hippocampal neurogenesis. Proc. Natl. Acad. Sci. USA 2010, 107:15625-15630.
41. Okun E., Griffioen K.J., Son T.G., Lee J.H., Roberts N.J., Mughal M.R., Hutchison E., Cheng A., Arumugam T.V., Lathia J.D., van Praag H., Mattson M.P. TLR2 activation inhibits embryonic neural progenitor cell proliferation. J. Neurochem. 2010, 114:462-474.
42. Okun E., Griffioen K.J., Mattson M.P. Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci. 2011, 34:269-281.
43. Okun E., Barak B., Saada-Madar R., Rothman S.M., Griffioen K.J., Roberts N., Castro K., Mughal M.R., Pita M.A., Stranahan A.M., Arumugam T.V., Mattson M.P. Evidence for a developmental role for TLR4 in learning and memory. PLoS One 2012, 7:e47522.
44. Ootsuka Y., Kulasekara K., de Menezes R.C., Blessing W.W. SR59230A, a beta-3 adrenoceptor antagonist, inhibits ultradian brown adipose tissue thermogenesis and interrupts associated episodic brain and body heating. American journal of physiology. Regulatory, Integrative, Comparative Physiology 2011, 301:R987-R994.
45. Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
46. Rolls A., Shechter R., London A., Ziv Y., Ronen A., Levy R., Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat. Cell Biol. 2007, 9:1081-1088.
47. Romanovsky A.A., Steiner A.A., Matsumura K. Cells that trigger fever. Cell Cycle 2006, 5:2195-2197.
48. Shechter R., Ronen A., Rolls A., London A., Bakalash S., Young M.J., Schwartz M. Toll-like receptor 4 restricts retinal progenitor cell proliferation. J. Cell Biol. 2008, 183:393-400.
49. Shechter R., London A., Kuperman Y., Ronen A., Rolls A., Chen A., Schwartz M. Hypothalamic neuronal toll-like receptor 2 protects against age-induced obesity. Sci. Rep. 2013, 3:1254.
50. Takeda K., Akira S. TLR signaling pathways. Semin. Immunol. 2004, 16:3-9.
51. Tang S.C., Lathia J.D., Selvaraj P.K., Jo D.G., Mughal M.R., Cheng A., Siler D.A., Markesbery W.R., Arumugam T.V., Mattson M.P. Toll-like receptor-4 mediates neuronal apoptosis induced by amyloid beta-peptide and the membrane lipid peroxidation product 4-hydroxynonenal. Exp. Neurol. 2008, 213:114-121.
52. Topkara V.K., Evans S., Zhang W., Epelman S., Staloch L., Barger P.M., Mann D.L. Therapeutic targeting of innate immunity in the failing heart. J. Mol. Cell Cardiol. 2011, 51:594-599.
53. Ubeda C., Lipuma L., Gobourne A., Viale A., Leiner I., Equinda M., Khanin R., Pamer E.G. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J. Exp. Med. 2012, 209:1445-1456.
54. Vallejo J.G. Role of toll-like receptors in cardiovascular diseases. Clin. Sci. (London) 2011, 121:1-10.
55. Vijay-Kumar M., Aitken J.D., Carvalho F.A., Cullender T.C., Mwangi S., Srinivasan S., Sitaraman S.V., Knight R., Ley R.E., Gewirtz A.T. Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science 2010, 328:228-231.
56. Wu Y., Li W., Zhou C., Lu F., Gao T., Liu Y., Cao J., Zhang Y. Ketamine inhibits lipopolysaccharide-induced astrocytes activation by suppressing TLR4/NF-kB pathway. Cell Physiol. Biochem. 2012, 30:609-617.
57. Yu L., Wang L., Chen S. Endogenous toll-like receptor ligands and their biological significance. J. Cell. Mol. Med. 2010, 14:2592-2603.
58. Zhang H., Yuan X., Jin P.F., Hou J.F., Wang W., Wei Y.J., Hu S. Alteration of parasympathetic/sympathetic ratio in the infarcted myocardium after Schwann cell transplantation modified electrophysiological function of heart: a novel antiarrhythmic therapy. Circulation 2010, 122:S193-S200.
59. Zhao J., Cannon B., Nedergaard J. Thermogenesis is beta3- but not beta1-adrenergically mediated in rat brown fat cells, even after cold acclimation. Am. J. Physiol. 1998, 275:R2002-R2011.