The biphasic and age-dependent impact of klotho on hallmarks of aging and skeletal muscle function

Elife. 2021 Apr 20:10:e61138. doi: 10.7554/eLife.61138.

Abstract

Aging is accompanied by disrupted information flow, resulting from accumulation of molecular mistakes. These mistakes ultimately give rise to debilitating disorders including skeletal muscle wasting, or sarcopenia. To derive a global metric of growing 'disorderliness' of aging muscle, we employed a statistical physics approach to estimate the state parameter, entropy, as a function of genes associated with hallmarks of aging. Escalating network entropy reached an inflection point at old age, while structural and functional alterations progressed into oldest-old age. To probe the potential for restoration of molecular 'order' and reversal of the sarcopenic phenotype, we systemically overexpressed the longevity protein, Klotho, via AAV. Klotho overexpression modulated genes representing all hallmarks of aging in old and oldest-old mice, but pathway enrichment revealed directions of changes were, for many genes, age-dependent. Functional improvements were also age-dependent. Klotho improved strength in old mice, but failed to induce benefits beyond the entropic tipping point.

Keywords: adeno-associated virus; computational biology; hallmarks of aging; klotho; mouse; muscle stem cells; regenerative medicine; sarcopenia; skeletal muscle; stem cells; systems biology.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age Factors
  • Aging / genetics
  • Aging / metabolism*
  • Aging / pathology
  • Animals
  • Dependovirus / genetics
  • Dependovirus / metabolism
  • Female
  • Gene Expression Regulation
  • Genetic Therapy
  • Genetic Vectors
  • Glucuronidase / genetics
  • Glucuronidase / metabolism*
  • HEK293 Cells
  • Humans
  • Klotho Proteins
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Muscle Strength
  • Muscle, Skeletal / metabolism*
  • Muscle, Skeletal / pathology
  • Muscle, Skeletal / physiopathology
  • Recovery of Function
  • Sarcopenia / genetics
  • Sarcopenia / metabolism*
  • Sarcopenia / physiopathology
  • Sarcopenia / therapy
  • Transcriptome

Substances

  • Glucuronidase
  • Klotho Proteins

Associated data

  • GEO/GSE156343
  • GEO/GSE164471