KLOTHO KL-VS heterozygosity is associated with diminished age-related neuroinflammation, neurodegeneration, and synaptic dysfunction in older cognitively unimpaired adults

Alzheimers Dement. 2024 Aug;20(8):5347-5356. doi: 10.1002/alz.13912. Epub 2024 Jun 21.

Abstract

Introduction: We examined whether the aging suppressor KLOTHO gene's functionally advantageous KL-VS variant (KL-VS heterozygosity [KL-VSHET]) confers resilience against deleterious effects of aging indexed by cerebrospinal fluid (CSF) biomarkers of neuroinflammation (interleukin-6 [IL-6], S100 calcium-binding protein B [S100B], triggering receptor expressed on myeloid cells [sTREM2], chitinase-3-like protein 1 [YKL-40], glial fibrillary acidic protein [GFAP]), neurodegeneration (total α-synuclein [α-Syn], neurofilament light chain protein), and synaptic dysfunction (neurogranin [Ng]).

Methods: This Alzheimer disease risk-enriched cohort consisted of 454 cognitively unimpaired adults (Mage = 61.5 ± 7.75). Covariate-adjusted multivariate regression examined relationships between age (mean-split[age ≥ 62]) and CSF biomarkers (Roche/NeuroToolKit), and whether they differed between KL-VSHET (N = 122) and non-carriers (KL-VSNC; N = 332).

Results: Older age was associated with a poorer biomarker profile across all analytes (Ps ≤ 0.03). In age-stratified analyses, KL-VSNC exhibited this same pattern (Ps ≤ 0.05) which was not significant for IL-6, S100B, Ng, and α-Syn (Ps ≥ 0.13) in KL-VSHET. Although age-related differences in GFAP, sTREM2, and YKL-40 were evident for both groups (Ps ≤ 0.01), the effect magnitude was markedly stronger for KL-VSNC.

Discussion: Higher levels of neuroinflammation, neurodegeneration, and synaptic dysfunction in older adults were attenuated in KL-VSHET.

Highlights: Older age was associated with poorer profiles across all cerebrospinal fluid biomarkers of neuroinflammation, neurodegeneration, and synaptic dysfunction. KLOTHO KL-VS non-carriers exhibit this same pattern, which is does not significantly differ between younger and older KL-VS heterozygotes for interleukin-6, S100 calcium-binding protein B, neurogranin, and total α-synuclein. Although age-related differences in glial fibrillary acidic protein, triggering receptor expressed on myeloid cells, and chitinase-3-like protein 1 are evident for both KL-VS groups, the magnitude of the effect is markedly stronger for KL-VS non-carriers. Higher levels of neuroinflammation, neurodegeneration, and synaptic dysfunction in older adults are attenuated in KL-VS heterozygotes.

Keywords: Alzheimer's disease; S100 calcium‐binding protein B; chitinase‐3‐like protein 1; glial fibrillary acidic protein; interleukin 6; neurogranin; protective factors; resilience; risk; triggering receptor expressed on myeloid cells; α‐synuclein.

Publication types

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

MeSH terms

  • Aged
  • Aging* / genetics
  • Alzheimer Disease / cerebrospinal fluid
  • Alzheimer Disease / genetics
  • Biomarkers* / cerebrospinal fluid
  • Chitinase-3-Like Protein 1* / cerebrospinal fluid
  • Chitinase-3-Like Protein 1* / genetics
  • Cohort Studies
  • Female
  • Glial Fibrillary Acidic Protein / cerebrospinal fluid
  • Glial Fibrillary Acidic Protein / genetics
  • Glucuronidase / cerebrospinal fluid
  • Glucuronidase / genetics
  • Heterozygote*
  • Humans
  • Interleukin-6 / cerebrospinal fluid
  • Interleukin-6 / genetics
  • Klotho Proteins*
  • Male
  • Membrane Glycoproteins
  • Middle Aged
  • Neurogranin / cerebrospinal fluid
  • Neurogranin / genetics
  • Neuroinflammatory Diseases / cerebrospinal fluid
  • Neuroinflammatory Diseases / genetics
  • Receptors, Immunologic / genetics
  • S100 Calcium Binding Protein beta Subunit / cerebrospinal fluid
  • S100 Calcium Binding Protein beta Subunit / genetics
  • alpha-Synuclein / cerebrospinal fluid
  • alpha-Synuclein / genetics

Substances

  • Klotho Proteins
  • Biomarkers
  • Chitinase-3-Like Protein 1
  • CHI3L1 protein, human
  • Glucuronidase
  • Interleukin-6
  • Receptors, Immunologic
  • TREM2 protein, human
  • S100 Calcium Binding Protein beta Subunit
  • S100B protein, human
  • Glial Fibrillary Acidic Protein
  • alpha-Synuclein
  • Neurogranin
  • IL6 protein, human
  • GFAP protein, human
  • Membrane Glycoproteins