BDNF modulates heart contraction force and long-term homeostasis through truncated TrkB.T1 receptor activation

Journal of Cell Biology

Volumn 210, Issue 6, 2015, Pages 1003-1012

  Fulgenzi, Gianluca ^a,b   Tomassoni Ardori, Francesco ^a   Babini, Lucia ^a   Becker, Jodi ^a   Barrick, Colleen ^a   Puverel, Sandrine ^a   Tessarollo, Lino ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; NEUROTROPHIN; PROTEIN TRKB.T1; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; NTRK2 PROTEIN, MOUSE; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CALCIUM SIGNALING; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; HEART MUSCLE CONTRACTILE FORCE; HEART MUSCLE CONTRACTILITY; HOMEOSTASIS; INNERVATION; MALE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CARDIAC MUSCLE CELL; CARDIOMYOPATHY; DEFICIENCY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; GENOTYPE; HEART CONTRACTION; ISOLATED HEART; KNOCKOUT MOUSE; METABOLISM; MUSCLE STRENGTH; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; TIME FACTOR; TRANSGENIC MOUSE;

ANIMALS; AUTOCRINE COMMUNICATION; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM SIGNALING; CARDIOMYOPATHIES; ENZYME ACTIVATION; GENOTYPE; ISOLATED HEART PREPARATION; MALE; MEMBRANE GLYCOPROTEINS; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE STRENGTH; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PARACRINE COMMUNICATION; PHENOTYPE; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84975886555     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201502100     Document Type: Article

References (40)

1. Agah, R., P.A. Frenkel, B.A. French, L.H. Michael, P.A. Overbeek, and M.D. Schneider. 1997. Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J. Clin. Invest. 100:169-179. http://dttp://dx.d.1172/JCI119509
2. Alva, J.A., A.C. Zovein, A. Monvoisin, T. Murphy, A. Salazar, N.L. Harvey, P. Carmeliet, and M.L. Iruela-Arispe. 2006. VE-Cadherin-Crerecombinase transgenic mouse: A tool for lineage analysis and gene deletion in endothelial cells. Dev. Dyn. 235:759-767. http://dttp://dx.d.1002/dvdy.20643
3. Anastasia, A., K. Deinhardt, S. Wang, L. Martin, D. Nichol, K. Irmady, J. Trinh, L. Parada, S. Rafii, B.L. Hempstead, and P. Kermani. 2014. Trkb signaling in pericytes is required for cardiac microvessel stabilization. PLoS ONE. 9:e87406. http://dttp://dx.d.1371/journal.pone.0087406
4. Arganda-Carreras, I., C.S. Sorzano, R. Marabini, J. Carazo, C. Ortiz-de- Solorzano, and J. Kybic. 2006. Consistent and elastic registration of histological sections using vector-spline regularization. In Computer Vision Approaches to Medical Image Analysis. Vol. 4241. R. Beichel, and M. Sonka, editors. Springer-Verlag Berlin Heidelberg, Berlin/Heidelberg. 85-95. http://dttp://dx.d.1007/11889762_8
5. Baydyuk, M., and B. Xu. 2014. BDNF signaling and survival of striatal neurons. Front. Cell. Neurosci. 8:254. http://dttp://dx.d.3389/fncel.2014.00254
6. 2+ current in ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 48:26-36. http://dttp://dx.d.1016/j.yjmcc.2009.07.026
7. 2+. Biochem. J. 306:445-451. http://dttp://dx.d.1042/bj3060445
8. Broadley, K.J. 1979. The Langendorff heart preparation-Reappraisal of its role as a research and teaching model for coronary vasoactive drugs. J. Pharmacol. Methods. 2:143-156. http://dttp://dx.d.1016/0160-5402(79)90038-X
9. Carim-Todd, L., K.G. Bath, G. Fulgenzi, S. Yanpallewar, D. Jing, C.A. Barrick, J. Becker, H. Buckley, S.G. Dorsey, F.S. Lee, and L. Tessarollo. 2009. Endogenous truncated TrkB.T1 receptor regulates neuronal complexity and TrkB kinase receptor function in vivo. J. Neurosci. 29:678-685. http://dttp://dx.d.1523/JNEUROSCI.5060-08.2009
10. Chao, M.V., R. Rajagopal, and F.S. Lee. 2006. Neurotrophin signalling in health and disease. Clin. Sci. 110:167-173. http://dttp://dx.d.1042/CS20050163
11. Chen, X., H. Ye, R. Kuruvilla, N. Ramanan, K.W. Scangos, C. Zhang, N.M. Johnson, P.M. England, K.M. Shokat, and D.D. Ginty. 2005. A chemical-genetic approach to studying neurotrophin signaling. Neuron. 46:13-21. http://dttp://dx.d.1016/j.neuron.2005.03.009
12. Clark, C.G., E.M. Hasser, D.L. Kunze, D.M. Katz, and D.D. Kline. 2011. Endogenous brain-derived neurotrophic factor in the nucleus tractus solitarius tonically regulates synaptic and autonomic function. J. Neurosci. 31:12318-12329. http://dttp://dx.d.1523/JNEUROSCI.0746-11.2011
13. Coppola, V., J. Kucera, M.E. Palko, J. Martinez-De Velasco, W.E. Lyons, B. Fritzsch, and L. Tessarollo. 2001. Dissection of NT3 functions in vivo by gene replacement strategy. Development. 128:4315-4327.
14. Donovan, M.J., M.I. Lin, P. Wiegn, T. Ringstedt, R. Kraemer, R. Hahn, S. Wang, C.F. Ibañez, S. Rafii, and B.L. Hempstead. 2000. Brain derived neurotrophic factor is an endothelial cell survival factor required for intramyocardial vessel stabilization. Development. 127:4531-4540.
15. Dorsey, S.G., C.L. Renn, L. Carim-Todd, C.A. Barrick, L. Bambrick, B.K. Krueger, C.W. Ward, and L. Tessarollo. 2006. In vivo restoration of physiological levels of truncated TrkB.T1 receptor rescues neuronal cell death in a trisomic mouse model. Neuron. 51:21-28. http://dttp://dx.d.1016/j.neuron.2006.06.009
16. Emanueli, C., M. Meloni, W. Hasan, and B.A. Habecker. 2014. The biology of neurotrophins: cardiovascular function. Handbook Exp. Pharmacol. 220:309-328. http://dttp://dx.d.1007/978-3-642-45106-5_12
17. Escandón, E., D. Soppet, A. Rosenthal, J.L. Mendoza-Ramírez, E. Szönyi, L.E. Burton, C.E. Henderson, L.F. Parada, and K. Nikolics. 1994. Regulation of neurotrophin receptor expression during embryonic and postnatal development. J. Neurosci. 14:2054-2068.
18. Feng, N., S. Huke, G. Zhu, C.G. Tocchetti, S. Shi, T. Aiba, N. Kaludercic, D.B. Hoover, S.E. Beck, J.L. Mankowski, et al. 2015. Constitutive BDNF/ TrkB signaling is required for normal cardiac contraction and relaxation. Proc. Natl. Acad. Sci. USA. 112:1880-1885. http://dttp://dx.d.1073/pnas.1417949112
19. Gao, S., D. Ho, D.E. Vatner, and S.F. Vatner. 2011. Echocardiography in mice. Curr. Protoc, Mouse Biol. 1:71-83.
20. Graciotti, L., J. Becker, A.L. Granata, A.D. Procopio, L. Tessarollo, and G. Fulgenzi. 2011. Dystrophin is required for the normal function of the cardio-protective KATP channel in cardiomyocytes. PLoS ONE. 6:e27034. http://dttp://dx.d.1371/journal.pone.0027034
21. Klein, R., D. Conway, L.F. Parada, and M. Barbacid. 1990. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell. 61:647-656. http://dttp://dx.d.1016/0092-8674(90)90476-U
22. Klein, R., R.J. Smeyne, W. Wurst, L.K. Long, B.A. Auerbach, A.L. Joyner, and M. Barbacid. 1993. Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell. 75:113- 122. http://dttp://dx.d.1016/S0092-8674(05)80088-1
23. Kockskämper, J., A.V. Zima, H.L. Roderick, B. Pieske, L.A. Blatter, and M.D. Bootman. 2008. Emerging roles of inositol 1,4,5-trisphosphate signaling in cardiac myocytes. J. Mol. Cell. Cardiol. 45:128-147. http://dttp://dx.d.1016/j.yjmcc.2008.05.014
24. Longo, F.M., and S.M. Massa. 2013. Small-molecule modulation of neurotrophin receptors: a strategy for the treatment of neurological disease. Nat. Rev. Drug Discov. 12:507-525. http://dttp://dx.d.1038/nrd4024
25. Lu, B., G. Nagappan, and Y. Lu. 2014. BDNF and synaptic plasticity, cognitive function, and dysfunction. Handbook Exp. Pharmacol. 220:223-250. http://dttp://dx.d.1007/978-3-642-45106-5_9
26. Mende, U., A. Kagen, A. Cohen, J. Aramburu, F.J. Schoen, and E.J. Neer. 1998. Transient cardiac expression of constitutively active Gaq leads to hypertrophy and dilated cardiomyopathy by calcineurin-dependent and independent pathways. Proc. Natl. Acad. Sci. USA. 95:13893-13898. http://dttp://dx.d.1073/pnas.95.23.13893
27. 2+ is loading- dependent. J. Biol. Chem. 269:7238-7242.
28. Nagahara, A.H., and M.H. Tuszynski. 2011. Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat. Rev. Drug Discov. 10:209- 219. http://dttp://dx.d.1038/nrd3366
29. Ohira, K., K.J. Homma, H. Hirai, S. Nakamura, and M. Hayashi. 2006. TrkB-T1 regulates the RhoA signaling and actin cytoskeleton in glioma cells. Biochem. Biophys. Res. Commun. 342:867-874. http://dttp://dx.d.1016/j.bbrc.2006.02.033
30. Rios, M., G. Fan, C. Fekete, J. Kelly, B. Bates, R. Kuehn, R.M. Lechan, and R. Jaenisch. 2001. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol. Endocrinol. 15:1748-1757. http://dttp://dx.d.1210/mend.15.10.0706
31. Rose, C.R., R. Blum, B. Pichler, A. Lepier, K.W. Kafitz, and A. Konnerth. 2003. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature. 426:74-78. http://dttp://dx.d.1038/nature01983
32. Rosenthal, A., and J.C. Lin. 2014. Modulation of neurotrophin signaling by monoclonal antibodies. Handbook Exp. Pharmacol. 220:497-512. http://dttp://dx.d.1007/978-3-642-45106-5_19
33. Scarisbrick, I.A., E.G. Jones, and P.J. Isackson. 1993. Coexpression of mRNAs for NGF, BDNF, and NT-3 in the cardiovascular system of the pre- and postnatal rat. J. Neurosci. 13:875-893.
34. Stoilov, P., E. Castren, and S. Stamm. 2002. Analysis of the human TrkB gene genomic organization reveals novel TrkB isoforms, unusual gene length, and splicing mechanism. Biochem. Biophys. Res. Commun. 290:1054- 1065. http://dttp://dx.d.1006/bbrc.2001.6301
35. Wan, R., L.A. Weigand, R. Bateman, K. Griffioen, D. Mendelowitz, and M.P. Mattson. 2014. Evidence that BDNF regulates heart rate by a mechanism involving increased brainstem parasympathetic neuron excitability. J. Neurochem. 129:573-580. http://dttp://dx.d.1111/jnc.12656
36. Wiese, S., S. Jablonka, B. Holtmann, N. Orel, R. Rajagopal, M.V. Chao, and M. Sendtner. 2007. Adenosine receptor A2A-R contributes to motoneuron survival by transactivating the tyrosine kinase receptor TrkB. Proc. Natl. Acad. Sci. USA. 104:17210-17215. http://dttp://dx.d.1073/pnas.0705267104
37. Wolska, B.M., and R.J. Solaro. 1996. Method for isolation of adult mouse cardiac myocytes for studies of contraction and microfluorimetry. Am. J. Physiol. 271:H1250-H1255.
38. Yang, J., C.J. Siao, G. Nagappan, T. Marinic, D. Jing, K. McGrath, Z.Y. Chen, W. Mark, L. Tessarollo, F.S. Lee, et al. 2009. Neuronal release of proBDNF. Nat. Neurosci. 12:113-115. http://dttp://dx.d.1038/nn.2244
39. Yanpallewar, S.U., C.A. Barrick, H. Buckley, J. Becker, and L. Tessarollo. 2012. Deletion of the BDNF truncated receptor TrkB.T1 delays disease onset in a mouse model of amyotrophic lateral sclerosis. PLoS ONE. 7:e39946. http://dttp://dx.d.1371/journal.pone.0039946
40. Zuccato, C., and E. Cattaneo. 2009. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 5:311-322. http://dttp://dx.d.1038/nrneurol.2009.54