The intracellular production and transport of energetic substrate adenosine triphosphate (ATP) produced by mitochondria is dependent on multiple factors. These include local metabolic demand, mitochondrial motility and intracellular location, mitochondrial intermembrane potential, bioenergy substrate diffusion within the cell cytosol, and energy transport to the cell nucleus, which itself does not contain any mitochondria. Herein, we demonstrate via cell-based experiment and scaling argument that intracellular bioenergy transport is readily compartmentalized into perinuclear and peripheral regions of the cell. We draw on direct fluorescence-based measurement of quantum dot tracking, high-resolution respirometry, mitochondrial dynamics, and intermembrane potential to assess intracellular quantum dot diffusion to define the intracellular milieu for small molecule transport, and chemical perturbations which challenge cells by altering bioenergetics states. We identify a heterogeneous environment for intracellular bioenergy transport, with a dominant feature being present: the intracellular bioenergy distribution in response to pharmacologically induced cell challenge is determined to be preservation of perinuclear mitochondrial ATP-linked respiration in order to preserve, maintain, or otherwise support bioenergy delivery to meet the metabolic requirements of the cell nucleus whereas there is a decrement in bioenergetic capacity in the cell periphery. This dynamic effect of motile intracellular bioenergy production yields efficient transport of ATP in the maintenance of cellular health.
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Research-Article
Compartmentalization of Bioenergetic Substrate Delivery in Intact Cells
David M. Eckmann,
David M. Eckmann
Department of Anesthesiology and Critical Care,
Perelman School of Medicine,
University of Pennsylvania,
John Morgan Building 305,
3620 Hamilton Walk,
Philadelphia, PA 19104
e-mail: eckmanndm@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
John Morgan Building 305,
3620 Hamilton Walk,
Philadelphia, PA 19104
e-mail: eckmanndm@uphs.upenn.edu
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Abhay Ranganathan,
Abhay Ranganathan
Department of Anesthesiology and Critical Care,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: abhay.ranganathan@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: abhay.ranganathan@uphs.upenn.edu
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Shawn Owiredu,
Shawn Owiredu
Department of Emergency Medicine,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: shawn.owiredu@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: shawn.owiredu@uphs.upenn.edu
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David H. Jang
David H. Jang
Department of Emergency Medicine,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: david.jang@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: david.jang@uphs.upenn.edu
Search for other works by this author on:
David M. Eckmann
Department of Anesthesiology and Critical Care,
Perelman School of Medicine,
University of Pennsylvania,
John Morgan Building 305,
3620 Hamilton Walk,
Philadelphia, PA 19104
e-mail: eckmanndm@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
John Morgan Building 305,
3620 Hamilton Walk,
Philadelphia, PA 19104
e-mail: eckmanndm@uphs.upenn.edu
Abhay Ranganathan
Department of Anesthesiology and Critical Care,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: abhay.ranganathan@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: abhay.ranganathan@uphs.upenn.edu
Shawn Owiredu
Department of Emergency Medicine,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: shawn.owiredu@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: shawn.owiredu@uphs.upenn.edu
David H. Jang
Department of Emergency Medicine,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: david.jang@uphs.upenn.edu
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: david.jang@uphs.upenn.edu
Contributed by the Heat Transfer Division of ASME for publication in the JOURNAL OF HEAT TRANSFER. Manuscript received August 28, 2018; final manuscript received November 22, 2018; published online March 27, 2019. Assoc. Editor: Milind A. Jog.
J. Heat Transfer. May 2019, 141(5): 052001 (8 pages)
Published Online: March 27, 2019
Article history
Received:
August 28, 2018
Revised:
November 22, 2018
Citation
Eckmann, D. M., Ranganathan, A., Owiredu, S., and Jang, D. H. (March 27, 2019). "Compartmentalization of Bioenergetic Substrate Delivery in Intact Cells." ASME. J. Heat Transfer. May 2019; 141(5): 052001. https://doi.org/10.1115/1.4042186
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