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Swim exercise in Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability, and protects against neurodegeneration.

Publication ,  Journal Article
Laranjeiro, R; Harinath, G; Hewitt, JE; Hartman, JH; Royal, MA; Meyer, JN; Vanapalli, SA; Driscoll, M
Published in: Proceedings of the National Academy of Sciences of the United States of America
November 2019

Regular physical exercise is the most efficient and accessible intervention known to promote healthy aging in humans. The molecular and cellular mechanisms that mediate system-wide exercise benefits, however, remain poorly understood, especially as applies to tissues that do not participate directly in training activity. The establishment of exercise protocols for short-lived genetic models will be critical for deciphering fundamental mechanisms of transtissue exercise benefits to healthy aging. Here we document optimization of a long-term swim exercise protocol for Caenorhabditis elegans and we demonstrate its benefits to diverse aging tissues, even if exercise occurs only during a restricted phase of adulthood. We found that multiple daily swim sessions are essential for exercise adaptation, leading to body wall muscle improvements in structural gene expression, locomotory performance, and mitochondrial morphology. Swim exercise training enhances whole-animal health parameters, such as mitochondrial respiration and midlife survival, increases functional healthspan of the pharynx and intestine, and enhances nervous system health by increasing learning ability and protecting against neurodegeneration in models of tauopathy, Alzheimer's disease, and Huntington's disease. Remarkably, swim training only during early adulthood induces long-lasting systemic benefits that in several cases are still detectable well into midlife. Our data reveal the broad impact of swim exercise in promoting extended healthspan of multiple C. elegans tissues, underscore the potency of early exercise experience to influence long-term health, and establish the foundation for exploiting the powerful advantages of this genetic model for the dissection of the exercise-dependent molecular circuitry that confers system-wide health benefits to aging adults.

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Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

November 2019

Volume

116

Issue

47

Start / End Page

23829 / 23839

Related Subject Headings

  • Swimming
  • Neuroprotection
  • Nervous System Physiological Phenomena
  • Muscles
  • Learning
  • Intestines
  • Caenorhabditis elegans
  • Animals
  • Adaptation, Physiological
 

Citation

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Laranjeiro, R., Harinath, G., Hewitt, J. E., Hartman, J. H., Royal, M. A., Meyer, J. N., … Driscoll, M. (2019). Swim exercise in Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability, and protects against neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America, 116(47), 23829–23839. https://doi.org/10.1073/pnas.1909210116
Laranjeiro, Ricardo, Girish Harinath, Jennifer E. Hewitt, Jessica H. Hartman, Mary Anne Royal, Joel N. Meyer, Siva A. Vanapalli, and Monica Driscoll. “Swim exercise in Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability, and protects against neurodegeneration.Proceedings of the National Academy of Sciences of the United States of America 116, no. 47 (November 2019): 23829–39. https://doi.org/10.1073/pnas.1909210116.
Laranjeiro R, Harinath G, Hewitt JE, Hartman JH, Royal MA, Meyer JN, et al. Swim exercise in Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability, and protects against neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America. 2019 Nov;116(47):23829–39.
Laranjeiro, Ricardo, et al. “Swim exercise in Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability, and protects against neurodegeneration.Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 47, Nov. 2019, pp. 23829–39. Epmc, doi:10.1073/pnas.1909210116.
Laranjeiro R, Harinath G, Hewitt JE, Hartman JH, Royal MA, Meyer JN, Vanapalli SA, Driscoll M. Swim exercise in Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability, and protects against neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America. 2019 Nov;116(47):23829–23839.
Journal cover image

Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

November 2019

Volume

116

Issue

47

Start / End Page

23829 / 23839

Related Subject Headings

  • Swimming
  • Neuroprotection
  • Nervous System Physiological Phenomena
  • Muscles
  • Learning
  • Intestines
  • Caenorhabditis elegans
  • Animals
  • Adaptation, Physiological