STRC AC1/CREB Alternative Hypothesis

Replacement for the NFAT-based sonogenetic approach, after critical review found that Ca2+ from MET channels does not reach the OHC soma where NFAT/calcineurin reside.

Why NFAT Fails

  1. Ca2+ from MET channels is trapped in stereocilia by millimolar buffers, PMCA2 pumps, mitochondrial barrier, and 4-6 mM oncomodulin
  2. NFATc4 nuclear translocation in OHCs observed ONLY during damage (noise, ototoxins)
  3. NFATc4 downstream targets in OHC: TNF, Caspase-8, Caspase-3 (apoptosis)
  4. NFATc4 knockout mice have normal hearing

The AC1/CREB Cascade

Sound → MET channels → Ca2+ (in stereocilia)
→ Calmodulin (in stereocilia)
→ AC1/ADCY1 (IN stereocilia — confirmed by immunolocalization)
→ cAMP (small molecule, diffuses freely past cuticular plate)
→ PKA (in soma)
→ CREB phosphorylation (Ser133)
→ CRE-dependent promoter → mini-STRC expression

Why AC1/CREB is Better

Problem with NFATSolution in AC1/CREB
Ca2+ doesn’t reach somaAC1 is IN stereocilia, converts Ca2+ to cAMP locally
Ca2+ is heavily bufferedcAMP is not buffered, diffuses freely
NFAT activation = apoptosisCREB = neuroplasticity, no death link
NFATc4 KO = normal hearingADCY1 mutations = deafness (essential gene)

Key Evidence

  • ADCY1 in stereocilia: Protein localized to cochlear hair cell stereocilia and nuclei (PubMed 24482543)
  • ADCY1 causes deafness: Recessive hearing impairment in humans and zebrafish from ADCY1 mutations
  • Ca2+-calmodulin activates AC1: Well-characterized biochemistry. AC1 is one of two CaM-activated adenylyl cyclases (with AC8)
  • CRE promoter: Standard responsive element (TGACGTCA), used in viral vectors in vivo, well-characterized

What Remains Unknown

  1. Does AC1 produce enough cAMP during normal hearing (not just loud sound)?
  2. Does cAMP from stereocilia reach the nucleus at sufficient concentration?
  3. Would a CRE-responsive promoter fire in OHCs? Never tested.
  4. Specificity: cAMP/CREB responds to many signals beyond sound. May have unwanted basal activity.
  5. All ODE parameters need re-derivation for AC1/cAMP/PKA/CREB kinetics.

Construct Design (Preliminary)

5' ITR (145 bp) + CRE-responsive promoter (~200 bp) + mini-STRC CDS (3,546 bp) + bGH polyA (250 bp) + 3' ITR (145 bp)
= ~4,286 bp (414 bp margin in AAV)

CRE promoter options:

  • 6xCRE + minimal promoter (standard, ~200 bp)
  • Hybrid CRE-SRE (as in Pan et al. 2018, higher specificity)

Speculative: DFNB16-Specific Calcium Leak

In Strc-/- mice, stereocilia lose horizontal top connectors by P15, bundle stiffness drops 60-74%. Possible that disrupted structure allows Ca2+ to leak into soma, making NFAT viable ONLY in diseased cells. If true: disease activates promoter, cure silences it. Perfect self-dosing.

No one has measured somatic Ca2+ in Strc-/- OHCs. Testable by calcium imaging in cochlear explants.

Next Steps

  1. Build ODE model for AC1/cAMP/PKA/CREB pathway with cochlear parameters
  2. Ask Dr. Holt: “Does MET-channel Ca2+ reach the soma? Would AC1/CRE be more realistic?”
  3. Search for ADCY1 expression levels in OHC transcriptomes (Liu et al. 2014, Sdata 2018)
  4. Design 6xCRE promoter construct
  5. Consider calcium imaging experiment in Strc-/- explants

Connections