Journal of Comparative Physiology B

, Volume 188, Issue 6, pp 929–937 | Cite as

Sources of Ca2+ for contraction of the heart tube of Tenebrio molitor (Coleoptera: Tenebrionidae)

  • Arnaldo Fim NetoEmail author
  • Rosana A. Bassani
  • Pedro X. de Oliveira
  • José W. M. Bassani
Original Paper


Insect and vertebrate hearts share the ability to generate spontaneously their rhythmic electrical activity, which triggers the fluid-propelling mechanical activity. Although insects have been used as models in studies on the impact of genetic alterations on cardiac function, there is surprisingly little information on the generation of the inotropic activity in their hearts. The main goal of this study was to investigate the sources of Ca2+ for contraction in Tenebrio molitor hearts perfused in situ, in which inotropic activity was assessed by the systolic variation of the cardiac luminal diameter. Increasing the pacing rate from 1.0 to 2.5 Hz depressed contraction amplitude and accelerated relaxation. To avoid inotropic interference of variations in spontaneous rate, which have been shown to occur in insect heart during maneuvers that affect Ca2+ cycling, experiments were performed under electrical pacing at near-physiological rates. Raising the extracellular Ca2+ concentration from 0.5 to 8 mM increased contraction amplitude in a manner sensitive to L-type Ca2+ channel blockade by D600. Inotropic depression was observed after treatment with caffeine or thapsigargin, which impair Ca2+ accumulation by the sarcoplasmic reticulum (SR). D600, but not inhibition of the sarcolemmal Na+/Ca2+ exchanger by KB-R7943, further depressed inotropic activity in thapsigargin-treated hearts. From these results, it is possible to conclude that in T. molitor heart, as in vertebrates: (a) inotropic and lusitropic activities are modulated by the heart rate; and (b) Ca2+ availability for contraction depends on both Ca2+ influx via L-type channels and Ca2+ release from the SR.


Insect heart Inotropic activity Stimulation rate Ca2+ L-type Ca2+ channels Sarcoplasmic reticulum 



Extracellular Ca2+ concentration


Fractional shortening


Heart rate


Na+–Ca2+ exchanger


Sarcoplasmic reticulum


Half-time of relaxation


Time to peak contraction amplitude



We are indebted to Ms. Elizângela S. Oliveira and Mr. Renato S. Moura (Center for Biomedical Engineering/UNICAMP) for technical support. This study was supported by the Conselho Nacional de Pesquisa e Desenvolvimento (CNPq), Grants no 302996/2011-7 (JWMB), no 155508/2010-5 and no 163911/2012-6 (AFN).


  1. Abraham DM, Wolf MJ (2013) Disruption of sarcoendoplasmic reticulum calcium ATPase function in Drosophila leads to cardiac dysfunction. PLoS One 8:e77785CrossRefGoogle Scholar
  2. Affolter H, Coronado R (1986) Sidedness of reconstituted calcium channels from muscle transverse tubules as determined by D600 and D890 blockade. Biophys J 49:767–771CrossRefGoogle Scholar
  3. Antoons G, Mubagwa K, Nevelsteen I, Sipido KR (2002) Mechanisms underlying the frequency dependence of contraction and [Ca2+]i transients in mouse ventricular myocytes. J Physiol 543:889–898CrossRefGoogle Scholar
  4. Bassani RA, Bassani JWM (2002) Contribution of Ca2+ transporters to relaxation in intact ventricular myocytes from developing rats. Am J Physiol Heart Circ Physiol 282:H2406–H2413CrossRefGoogle Scholar
  5. Bassani JWM, Bassani RA, Bers DM (1993) Twitch-dependent SR Ca accumulation and release in rabbit ventricular myocytes. Am J Physiol Cell Physiol 265:C533–C540CrossRefGoogle Scholar
  6. Bassani JWM, Bassani RA, Bers DM (1994) Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476:279–293CrossRefGoogle Scholar
  7. Bassani RA, Mattiazzi A, Bers DM (1995) CaMKII is responsible for activity-dependent acceleration of relaxation in rat ventricular myocytes. Am J Physiol Heart Circ Physiol 268:H703–H712CrossRefGoogle Scholar
  8. Bassani RA, Gilioli R, Oliveira ES, Hoehr NF (2012) Blood calcium levels in immature rats: influence of extracellular calcium concentration on myocardial calcium handling. Exp Anim 61:399–405CrossRefGoogle Scholar
  9. Bers DM (2002) Cardiac excitation–contraction coupling. Nature 415:198–205CrossRefGoogle Scholar
  10. Bers DM, Bassani RA, Bassani JWM, Baudet S, Hryshko LV (1993) Paradoxical twitch potentiation after rest in cardiac muscle: increased fractional release of SR calcium. J Mol Cell Cardiol 25:1047–1057CrossRefGoogle Scholar
  11. Bodmer R, Venkatesh TV (1998) Heart development in Drosophila and vertebrates: conservation of molecular mechanisms. Dev Genet 22:181–186CrossRefGoogle Scholar
  12. Burkhardt S, van Eif V, Garric L, Chistoffels VM, Bakkers J (2017) On the evolution of the cardiac pacemaker. J Cardiovasc Dev Dis 4:4. CrossRefGoogle Scholar
  13. Choma MA, Suter MJ, Vakoc BJ, Bouma BE, Tearney GJ (2011) Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems. Dis Model Mech 4:411–420CrossRefGoogle Scholar
  14. Chowanski S, Rosinski G (2018) Myotropic effects of cholinergic muscarinic agonists and antagonists in the beetle Tenebrio molitor L. Curr Pharm Biotechnol. CrossRefGoogle Scholar
  15. Davia K, Davies CH, Harding SE (1997) Effects of inhibition of sarcoplasmic reticulum calcium uptake on contraction of myocytes isolated from failing human ventricle. Cardiovasc Res 33:88–97CrossRefGoogle Scholar
  16. Fabiato A (1982) Calcium release in skinned cardiac cells: variations with species, tissues, and development. Fed Proc 41:2238–2244PubMedGoogle Scholar
  17. Feliciano DF, Bassani RA, Oliveira PX, Bassani JWM (2011) Pacemaker activity in the insect (T. molitor) heart: role of the sarcoplasmic reticulum. Am J Physiol Regul Integr Comp Physiol 301:R1838–R1845CrossRefGoogle Scholar
  18. Frolov RV, Singh S (2012) Inhibition of ion channels and heartbeat in Drosophila by selective COX-2 inhibitor SC-791. PLoS One 7:e38759CrossRefGoogle Scholar
  19. Gwathmey JK, Morgan JP (1991) Calcium handling in myocardium from amphibian, avian, and mammalian species: the search for two components. J Comp Physiol B 161:19–25CrossRefGoogle Scholar
  20. Hertel W, Pass G (2002) An evolutionary treatment of the morphology and physiology of circulatory organs in insects. Comp Biochem Physiol A Mol Integr Physiol 133:555–575CrossRefGoogle Scholar
  21. Jennings T, Ringo J, Dowse H (2009) The relationship of heart function to temperature in Drosophila melanogaster and its heritability. J Exp Zool A Ecol Genet Physiol 311:689–696CrossRefGoogle Scholar
  22. Koch-Weser J, Blinks JR (1963) The influence of the interval between beats on myocardial contractility. Pharmacol Rev 15:601–652PubMedGoogle Scholar
  23. Lin N, Badie N, Yu L, Abraham D, Cheng H, Bursac N, Rockman HA, Wolf MJ (2011) A method to measure myocardial calcium handling in adult Drosophila. Circ Res 108:1306–1315CrossRefGoogle Scholar
  24. Ma L, Bradu A, Podoleanu AG, Bloor JW (2010) Arrhythmia caused by a Drosophila tropomyosin mutation is revealed using a novel optical coherence tomography instrument. PLoS One 5:e14348CrossRefGoogle Scholar
  25. Magny EG, Pueyo JI, Pearl FM, Cespedes MA, Niven JE, Bishop SA, Couso JP (2013) Conserved regulation of cardiac calcium uptake by peptides encoded in small open reading frames. Science 341:1116–1120CrossRefGoogle Scholar
  26. Maier LS, Bers DM (2007) Role of Ca2+/calmodulin protein kinase (CaMK) in excitation–contraction coupling in the heart. Cardiovasc Res 73:631–640CrossRefGoogle Scholar
  27. Maier LS, Bers DM, Pieske B (2000) Differences in Ca2+-handling and sarcoplasmic reticulum Ca2+-content in isolated rat and rabbit myocardium. J Mol Cell Cardiol 32:2249–2258CrossRefGoogle Scholar
  28. Malloy CA, Ritter K, Robinson J, English C, Cooper RL (2015) Pharmacological identification of cholinergic receptor subtypes on Drosophila melanogaster larval heart. J Comp Physiol B 186:45–57CrossRefGoogle Scholar
  29. Markou T, Theophilidis G (2000) The pacemaker activity generating the intrinsic myogenic contraction of the dorsal vessel of Tenebrio molitor (Coleoptera). J Exp Biol 203:3471–3483PubMedGoogle Scholar
  30. Ocorr K, Perrin L, Lim HY, Qian L, Wu X, Bodmer R (2007) Genetic control of heart function and aging in Drosophila. Trends Cardiovasc Med 17:177–182CrossRefGoogle Scholar
  31. Pacholska-Bogalska J, Szymczak M, Marciniak P, Walkowiak-Nowicka K, Rosiński G (2018) Heart mechanical and hemodynamic parameters of a beetle, Tenebrio molitor, at selected ages. Arch Insect Biochem Physiol 2018:e21474CrossRefGoogle Scholar
  32. Piazza N, Wessells RJ (2011) Drosophila models of cardiac disease. Prog Mol Biol Transl Sci 100:155–210CrossRefGoogle Scholar
  33. Pieske B, Maier LS, Bers DM, Hasenfuss G (1999) Ca2+ handling and sarcoplasmic reticulum Ca2+ content in isolated failing and nonfailing human myocardium. Circ Res 85:38–46CrossRefGoogle Scholar
  34. Sagara Y, Fernandez-Belda F, de Meis L, Inesi G (1992) Characterization of the inhibition of intracellular Ca2+ transport ATPases by thapsigargin. J Biol Chem 267:12606–12613PubMedGoogle Scholar
  35. Santalla M, Valverde CA, Harnichar E, Lacunza E, Aguilar-Fuentes J, Mattiazzi A, Ferrero P (2014) Aging and CaMKII alter intracellular Ca2+ transients and heart rhythm in Drosophila melanogaster. PLoS One 9:e101871CrossRefGoogle Scholar
  36. Sanyal S, Jennings T, Dowse H, Ramaswami M (2006) Conditional mutations in SERCA, the sarco-endoplasmic reticulum Ca2+-ATPase, alter heart rate and rhythmicity in Drosophila. J Comp Physiol B 176:253–263CrossRefGoogle Scholar
  37. Sherwood L, Klandorf H, Yancey P (2012) Animal physiology: from genes to organisms, 2nd edn. Brooks/Cole, BelmontGoogle Scholar
  38. Vinogradova TM, Brochet DX, Sirenko S, Li Y, Spurgeon H, Lakatta EG (2010) Sarcoplasmic reticulum Ca2+ pumping kinetics regulates timing of local Ca2+ releases and spontaneous beating rate of rabbit sinoatrial node pacemaker cells. Circ Res 107:767–775CrossRefGoogle Scholar
  39. Vornanen M, Shiels HA, Farrell AP (2002) Plasticity of excitation–contraction coupling in fish cardiac myocytes. Comp Biochem Physiol A Mol Integr Physiol 132:827–846CrossRefGoogle Scholar
  40. Watano T, Kimura J, Morita T, Nakanishi H (1996) A novel antagonist, No. 7943, of the Na+/Ca2+ exchange current in guinea-pig cardiac ventricular cells. Br J Pharmacol 119:555–563CrossRefGoogle Scholar
  41. Wendt IR, Stephenson DG (1983) Effects of caffeine on Ca-activated force production in skinned cardiac and skeletal muscle fibres of the rat. Pflugers Arch 398:210–216CrossRefGoogle Scholar
  42. Wolf MJ, Amrein H, Izatt JA, Choma MA, Reedy MC, Rockman HA (2006) Drosophila as a model for the identification of genes causing adult human heart disease. Proc Natl Acad Sci USA 103:1394–1399CrossRefGoogle Scholar
  43. Zornik E, Paisley K, Nichols R (1999) Neural transmitters and a peptide modulate Drosophila heart rate. Peptides 20:45–51CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biomedical Engineering, School of Electrical and Computer Engineering, and Center for Biomedical EngineeringUniversity of Campinas (UNICAMP)CampinasBrazil

Personalised recommendations