The DNA Repair Enzyme That Moonlights in RNA

The Unusual Story of Endonuclease V

A remarkable family of molecular guardians with surprising dual functions across different organisms

Introduction: A Tiny Cellular Guardian With a Dual Identity

In the bustling metropolis of a living cell, where genetic information is constantly under threat, a remarkable family of molecular guardians works tirelessly to maintain order. Among these protective proteins exists endonuclease V (EndoV), an enzyme full of surprises. Initially discovered as a bacterial DNA repair specialist, EndoV was thought to have a straightforward job: finding and removing damaged DNA bases before they could cause harmful mutations. But as scientists dug deeper, they uncovered a startling secret—this versatile enzyme also operates in the world of RNA, suggesting functions far beyond what was initially imagined 1 4 .

The story of Endonuclease V is one of scientific rediscovery and evolving understanding. For decades following its initial identification in 1977, researchers believed they knew what EndoV did. Then, twist after twist revealed that this enzyme operates differently across species, with distinct roles in prokaryotes versus eukaryotes, and possesses unexpected talents that have reshaped our understanding of cellular maintenance 1 .

This is the story of an unusual DNA repair enzyme that turned out to be much more than first meets the eye.

What is Endonuclease V?

Historical Background and Discovery

The Endonuclease V story begins in the laboratory of Stuart Linn at the University of California, Berkeley, where in 1977 it was identified as the "fifth endonuclease" in Escherichia coli (E. coli) 1 . Initially, researchers characterized it as an enzyme that could nick DNA at various damaged sites, including those caused by ultraviolet light or abnormal bases 1 . The corresponding gene was named nfi 1 .

1977

Endonuclease V discovered as the "fifth endonuclease" in E. coli

1990s

Identified as deoxyinosine 3' endonuclease by Kow and Weiss

2009

Crystal structure of T. maritima EndoV solved

2013

Human EndoV discovered to be an inosine-specific ribonuclease

The Deamination Problem EndoV Addresses

To understand EndoV's job, we must first appreciate the problem it solves: deamination, a common type of DNA damage. Deamination occurs when the amino groups (-NH₂) on DNA bases are removed and replaced with keto groups (=O), fundamentally changing their base-pairing properties 1 .

Causes of Deamination
  • Nitrosative stress from reactive nitrogen species generated during inflammation or infection 2 5
  • Hydrolytic damage from simple water exposure 1
Consequences of Deamination

When adenine loses its amino group, it becomes hypoxanthine, which pairs with cytosine instead of thymine 1 2 . Similarly, cytosine deamination creates uracil, which pairs with adenine instead of guanine 1 . If left unrepaired, these changes lead to mutations during DNA replication, potentially contributing to diseases like cancer 2 .

Common DNA Base Deaminations and Their Consequences
Original Base Deaminated Product Pairs With Resulting Mutation
Adenine (A) Hypoxanthine (Hx) Cytosine (C) A:T → G:C
Cytosine (C) Uracil (U) Adenine (A) G:C → A:T
Guanine (G) Xanthine (X) - Mutagenic/Blocks replication

The Unique Mechanism of Endonuclease V

How EndoV Recognizes and Repairs Damage

What makes EndoV unusual is its repair mechanism. Unlike many DNA repair enzymes that remove damaged bases, EndoV takes a different approach. It cleaves the DNA backbone specifically at the second phosphodiester bond 3' to the lesion 1 2 . This creates a nick with 3'-hydroxyl and 5'-phosphate ends, but leaves the damaged nucleotide in place 1 . This distinctive cleavage pattern—an offset nick one nucleotide downstream from the damage—is a signature feature of EndoV 2 .

This repair pathway, known as Alternative Excision Repair (AER), is biochemically distinct from the more familiar Base Excision Repair (BER) and Nucleotide Excision Repair (NER) pathways 9 . While BER involves removing the damaged base itself via glycosylase activity, and NER removes a segment containing the damage, AER simply nicks the DNA strand next to the lesion, requiring additional enzymes to complete the repair process 9 .

EndoV Cleavage Mechanism
A
Normal Adenine
Hx
Hypoxanthine
Cleavage
EndoV Action

EndoV cleaves at the second phosphodiester bond 3' to the deaminated base (hypoxanthine)

The PYIP Wedge: EndoV's Structural Secret Weapon

The 2009 crystal structure of Thermotoga maritima EndoV bound to DNA revealed the molecular secrets behind its function 2 . Researchers discovered a remarkable structural feature: a PYIP wedge motif (named for its proline-tyrosine-isoleucine-proline amino acid sequence) that acts as a minor-groove damage sensor 2 .

Functions of the PYIP Wedge Motif
  • Separates DNA strands at the lesion site by inserting into the DNA helix 2
  • Recognizes helical distortions caused by base damage 2
  • Pushes the base opposite the lesion partly out of the DNA duplex 2

The tyrosine residue (Tyr80) in this motif stacks against the base adjacent to the lesion and helps stabilize the distorted DNA structure 2 . Mutations in this tyrosine severely compromise EndoV's ability to bind and process damaged DNA, highlighting its importance 2 .

Recognition Pocket Features

Meanwhile, the damaged base itself is rotated approximately 90 degrees into a specialized recognition pocket about 8Å from the catalytic site 2 . This recognition pocket is lined with hydrophobic residues that interact with the damaged base, providing specificity for the repair process 2 .

90° Rotation
Recognition Pocket
Hydrophobic Residues

A Tale of Two Kingdoms: Prokaryotic vs. Eukaryotic EndoV

One of the most fascinating aspects of EndoV biology is the dramatic functional shift between prokaryotic and eukaryotic versions of the enzyme.

Bacterial EndoV: A DNA Repair Specialist

In bacteria like E. coli, EndoV functions primarily as a DNA repair enzyme with remarkably broad specificity 8 9 . While its main substrate appears to be deaminated adenine (hypoxanthine), it can also recognize and process:

  • Uracil from deaminated cytosine 9
  • Abasic sites (where a base is missing) 8
  • Base mismatches 8
  • Flap and pseudo-Y DNA structures 8
  • Small insertions/deletions 8

This broad substrate range reflects EndoV's general ability to recognize helical distortions in DNA rather than specific chemical lesions 2 .

Eukaryotic EndoV: An RNA Processing Enzyme

The big surprise came when researchers discovered that mammalian EndoV, including the human version, shows little activity on DNA but instead functions as an inosine-specific ribonuclease 4 5 . This represents a dramatic evolutionary shift in function.

Human EndoV:

  • Localizes to cytoplasm and nucleoli rather than being predominantly nuclear 4 5
  • Cleaves RNA containing inosine with high efficiency 4
  • Shows minimal activity on inosine-containing DNA 5

This suggests that in higher organisms, EndoV has been repurposed for RNA metabolism rather than DNA repair . Since inosine in RNA is frequently introduced by specific editing enzymes (ADARs) as a normal regulatory mechanism, this implies EndoV might play a role in processing edited RNAs or quality control of RNA molecules 4 5 .

Comparison of Prokaryotic and Eukaryotic Endonuclease V

Feature Prokaryotic EndoV Eukaryotic EndoV
Primary substrate DNA RNA
Cellular localization Nuclear Cytoplasmic/Nucleolar
Main function DNA repair RNA metabolism
Cofactor requirement Mg²⁺ or Mn²⁺ Mg²⁺ or Mn²⁺
Cleavage site 2nd phosphodiester bond 3' to lesion 2nd phosphodiester bond 3' to inosine
Biological role Genome maintenance RNA processing/quality control?
Substrate Preference Across Organisms
E. coli EndoV
DNA Preference
T. brucei EndoV
Mixed Preference
Human ENDOV
RNA Preference

In-Depth Look: A Key Experiment Revealing EndoV's RNA Talents

Background and Rationale

For years, scientists were puzzled by the human version of EndoV. The enzyme was highly conserved evolutionarily, yet recombinant human ENDOV showed little activity on inosine-containing DNA—supposedly its primary substrate 4 . This paradox continued until 2013, when researchers from Norway and Japan independently made a startling discovery: human EndoV is actually an inosine-specific ribonuclease 4 .

The critical clue came from cellular localization studies. When researchers fused human EndoV to green fluorescent protein, they observed that it wasn't located in the nucleus as expected for a DNA repair enzyme. Instead, it was found in the cytoplasm and nucleoli—compartments rich in RNA 4 . This spatial clue prompted scientists to question whether human EndoV might actually target RNA instead of DNA.

Experimental Approach
  1. Protein Purification: Researchers expressed and purified recombinant human ENDOV and E. coli EndoV from bacterial systems 4 .
  2. Substrate Design: They designed and synthesized both DNA and RNA oligonucleotides containing inosine at specific positions 4 .
  3. Activity Assays: The purified enzymes were incubated with various substrates under different conditions 4 .
  4. Product Analysis: Reaction products were separated using polyacrylamide gel electrophoresis 4 .
  5. Mutagenesis Studies: Researchers created specific mutations in conserved amino acid residues 4 .

Results and Analysis

The experiments yielded clear and compelling results:

  • Human ENDOV efficiently cleaved RNA substrates containing inosine but showed minimal activity on DNA substrates with inosine 4 .
  • E. coli EndoV cleaved both DNA and RNA substrates, demonstrating that both prokaryotic and eukaryotic enzymes recognize inosine, but with different nucleic acid preferences 4 .
  • Both enzymes cleaved at the second phosphodiester bond 3' to the inosine in RNA, the same site they target in DNA 4 .
  • Mutation of catalytic residues (aspartate in the DEDD motif) completely abolished RNA cleavage activity, confirming that the observed activity was intrinsic to EndoV and not a contamination artifact 4 .
Cleavage Efficiency of EndoV Enzymes on Different Substrates
Enzyme ssRNA with inosine dsRNA with inosine ssDNA with inosine dsDNA with inosine
E. coli EndoV ++ ++ +++ +++
Human ENDOV +++ ++ - -
T. brucei EndoV +++ - + -

Key: (+++) Strong activity, (++) Moderate activity, (+) Weak activity, (-) No detectable activity
Data compiled from 4 7

Scientific Importance

This discovery fundamentally changed our understanding of EndoV's biological role and evolutionary conservation. It revealed that:

  1. Evolution repurposes conserved enzymes for new functions, as demonstrated by the shift from DNA repair in prokaryotes to RNA metabolism in eukaryotes 4 .
  2. Cellular localization provides critical clues about protein function—human EndoV's cytoplasmic and nucleolar localization hinted at its RNA-related function 4 .
  3. The same structural fold can recognize similar lesions in different nucleic acids, demonstrating evolutionary economy 4 .

The findings opened new research directions into EndoV's potential roles in RNA quality control and the metabolism of inosine-containing RNAs produced by editing enzymes 4 5 .

The Scientist's Toolkit: Key Research Reagents

Studying an enzyme as versatile as EndoV requires specialized reagents and tools. Here are some essential components of the EndoV research toolkit:

Reagent/Tool Function/Application Examples/Specifics
Recombinant EndoV proteins Biochemical characterization of enzyme activity E. coli EndoV, human ENDOV, T. maritima EndoV 4 8
Oligonucleotide substrates Testing enzyme specificity and kinetics DNA/RNA with inosine, abasic sites, mismatches 4 7
Site-directed mutants Identifying critical residues for catalysis D35A (E. coli), D52A (human) catalytic mutants 4 5
Metal cofactors Essential for catalytic activity Mg²⁺, Mn²⁺ 4
Crystallization reagents Structural studies of enzyme-substrate complexes Used to solve T. maritima EndoV-DNA structures 2

Conclusion: The Continuing Mystery of Endonuclease V

The story of Endonuclease V continues to evolve. While we've made significant progress in understanding its molecular mechanisms and biochemical activities, many questions remain unanswered, particularly for the eukaryotic versions of the enzyme.

Unanswered Questions
  • What is the precise biological role of human ENDOV in RNA metabolism?
  • Does it function in quality control to eliminate improperly edited RNAs?
  • Does it participate in the maturation of ribosomal RNA in the nucleolus?
  • How is its activity regulated in cells?
Recent Findings

Recent research suggests that human EndoV's activity may be controlled by ATP levels and its recruitment to cytoplasmic stress granules under certain conditions 5 .

What is clear is that Endonuclease V represents a fascinating example of evolutionary adaptation. From its origins as a DNA repair enzyme in bacteria to its repurposing as an RNA-processing enzyme in humans, this unusual enzyme continues to surprise and delight scientists with its versatility and conservation across domains of life.

As research continues, Endonuclease V may well yield new insights into cellular maintenance mechanisms, the evolutionary repurposing of protein folds, and potentially even new biotechnology applications in mutation detection and DNA manipulation 1 . For an enzyme that was discovered over four decades ago, Endonuclease V continues to reveal new secrets about the intricate workings of the cell.

References