Morpho-functional characterization of the systemic venous pole of the reptile heart

Sci Rep. 2017 Jul 27;7(1):6644. doi: 10.1038/s41598-017-06291-z.

Abstract

Mammals evolved from reptile-like ancestors, and while the mammalian heart is driven by a distinct sinus node, a sinus node is not apparent in reptiles. We characterized the myocardial systemic venous pole, the sinus venosus, in reptiles to identify the dominant pacemaker and to assess whether the sinus venosus remodels and adopts an atrium-like phenotype as observed in mammals. Anolis lizards had an extensive sinus venosus of myocardium expressing Tbx18. A small sub-population of cells encircling the sinuatrial junction expressed Isl1, Bmp2, Tbx3, and Hcn4, homologues of genes marking the mammalian sinus node. Electrical mapping showed that hearts of Anolis lizards and Python snakes were driven from the sinuatrial junction. The electrical impulse was delayed between the sinus venosus and the right atrium, allowing the sinus venosus to contract and aid right atrial filling. In proximity of the systemic veins, the Anolis sinus venosus expressed markers of the atrial phenotype Nkx2-5 and Gja5. In conclusion, the reptile heart is driven by a pacemaker region with an expression signature similar to that of the immature sinus node of mammals. Unlike mammals, reptiles maintain a sinuatrial delay of the impulse, allowing the partly atrialized sinus venosus to function as a chamber.

MeSH terms

  • Alligators and Crocodiles / anatomy & histology
  • Alligators and Crocodiles / physiology
  • Animals
  • Boidae / anatomy & histology
  • Boidae / physiology
  • Bone Morphogenetic Protein 2 / genetics
  • Connexins / genetics
  • Electrophysiological Phenomena*
  • Gene Expression
  • Heart / anatomy & histology
  • Heart / physiology*
  • Homeobox Protein Nkx-2.5 / genetics
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / genetics
  • LIM-Homeodomain Proteins / genetics
  • Lizards / anatomy & histology
  • Lizards / physiology
  • Muscle Proteins / genetics*
  • Myocardium / metabolism
  • Reptiles / anatomy & histology*
  • Reptiles / metabolism
  • Reptiles / physiology*
  • Reptilian Proteins / genetics
  • T-Box Domain Proteins / genetics
  • Transcription Factors / genetics
  • Turtles / anatomy & histology
  • Turtles / physiology

Substances

  • Bone Morphogenetic Protein 2
  • Connexins
  • Homeobox Protein Nkx-2.5
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • LIM-Homeodomain Proteins
  • Muscle Proteins
  • Reptilian Proteins
  • T-Box Domain Proteins
  • Transcription Factors
  • connexin 40
  • insulin gene enhancer binding protein Isl-1