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PreprintCited by 10Trace Elements in HealthMuscle Physiology and DisordersIron Metabolism and Disorders

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Cysteine Rich Intestinal Protein 2 is a copper-responsive regulator of skeletal muscle differentiation

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Verdejo-Torres, Odette, Klein, David C., Novoa-Aponte, Lorena, Carrazco-Carrillo, Jaime, Bonilla-Pinto, Denzel, Rivera, Antonio, Fitisemanu, Fa’alataitaua, Jiménez-González, Martha L., Flinn, Lyra, Pezacki, Aidan T., Lanzirotti, Antonio, Ortiz-Frade, Luis Antonio, Chang, Christopher J., Navea, Juan G., Blaby-Haas, Crysten, Hainer, Sarah J., Padilla-Benavides, Teresita·2024·PLoS Genetics
DOI 10.1101/2024.05.03.592485PMC PMC11671023

Preprint — published as 10.1371/journal.pgen.1011495 · Paper page

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Abstract

Copper (Cu) is an essential trace element required for respiration, neurotransmitter synthesis, oxidative stress response, and transcriptional regulation. Imbalance in Cu homeostasis can lead to several pathological conditions, affecting neuronal, cognitive, and muscular development. Mechanistically, Cu and Cu-binding proteins (Cu-BPs) have an important but underappreciated role in transcription regulation in mammalian cells. In this context, our lab investigates the contributions of novel Cu-BPs in skeletal muscle differentiation using murine primary myoblasts. Through an unbiased synchrotron X-ray fluorescence-mass spectrometry (XRF/MS) metalloproteomic approach, we identified the murine cysteine rich intestinal protein 2 (mCrip2) in a sample that showed enriched Cu signal, which was isolated from differentiating primary myoblasts derived from mouse satellite cells. Immunolocalization analyses showed that mCrip2 is abundant in both nuclear and cytosolic fractions. Thus, we hypothesized that mCrip2 might have differential roles depending on its cellular localization in the skeletal muscle lineage. mCrip2 is a LIM-family protein with 4 conserved Zn 2+ -binding sites. Homology and phylogenetic analyses showed that mammalian Crip2 possesses histidine residues near two of the Zn 2+ -binding sites (CX2C-HX2C) which are potentially implicated in Cu + -binding and competition with Zn 2+ . Biochemical characterization of recombinant human hsCRIP2 revealed a high Cu + -binding affinity for two and four Cu + ions and limited redox potential. Functional characterization using CRISPR/Cas9-mediated deletion of mCrip2 in primary myoblasts did not impact proliferation, but impaired myogenesis by decreasing the expression of differentiation markers, possibly attributed to Cu accumulation. Transcriptome analyses of proliferating and differentiating mCrip2 KO myoblasts showed alterations in mRNA processing, protein translation, ribosome synthesis, and chromatin organization. CUT&RUN analyses showed that mCrip2 associates with a select set of gene promoters, including MyoD1 and metallothioneins , acting as a novel Cu-responsive or Cu-regulating protein. Our work demonstrates novel regulatory functions of mCrip2 that mediate skeletal muscle differentiation, presenting new features of the Cu-network in myoblasts.

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Metadata

Authors
Verdejo-Torres, O., Klein, D. C., Novoa-Aponte, L., Carrazco-Carrillo, J., Bonilla-Pinto, D., Rivera, A., Fitisemanu, F., Jiménez-González, M. L., Flinn, L., Pezacki, A. T., Lanzirotti, A., Ortiz-Frade, L. A., Chang, C. J., Navea, J. G., Blaby-Haas, C., Hainer, S. J., & Padilla-Benavides, T.
Affiliations
  • University of Pittsburgh (US)
  • Wesleyan University (US)
  • Center of Research and Technologic Development in Electrochemistry (MX)
  • Skidmore College (US)
  • Princeton University (US)
  • University of Chicago (US)
ORCID
Venue
PLoS Genetics
Publisher
openRxiv
Published
2024-05-05
Volume
20
Issue
12
Pages
e1011495-e1011495
ISSN
1553-7390 (ISSN-L)
DOI
10.1101/2024.05.03.592485
PMC
PMC11671023
OpenAlex
W4405092371
Cited by
10
References
1
Citations by year
2026: 7 · 2025: 2 · 2024: 1
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2.67
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journal article
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en
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cc-by
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  • Knowledge@UChicago (University of Chicago) (submittedVersion)
  • University of Chicago (cc-by)
Funders
  • National Science Foundation (DEAC02-05CH11231, S10OD028483, 1634415, DE-AC02–06CH11357, R35GM133732)
  • U.S. Department of Energy (DE‐ AC02‐06CH11357, -AC02-05CH11231, AC02‐06CH11357, 05CH11231, DE AC02 05CH11231, 06CH11357, DE-AC02-)
  • Camille and Henry Dreyfus Foundation
  • University of Chicago (DE-AC02-06CH11357)
  • Canadian Institute for Advanced Research
  • University of Pittsburgh (SCR 022735, S10OD028483)
  • Worcester Polytechnic Institute
  • National Institutes of Health (DE-AC02–05CH11231, 1s10od028483-01a1, DE-AC02–06CH11357)
  • Office of Science (AC02‐06CH11357, DEAC02–05CH11231, AC02-05CH11231, DE-AC02, 05CH11231, 06CH11357, DE-AC02-06CH11357)
  • Center for Research Computing, University of Pittsburgh (SCR_022735)
  • National Institute of General Medical Sciences (GM-79465, R01GM079465, R35GM133732)
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS-R01AR077578, DE-AC02-06CH11357, R01AR077578)
  • Basic Energy Sciences (DE-AC02, 05CH11231, DE-AC02-05CH11231., DE-AC- 02-06CH11357, AC02‐06CH11357, AC02–05CH11231, 06CH11357)
  • Children's Hospital of Pittsburgh
  • Argonne National Laboratory (DE- AC02-06-CH11357, DE-AC02, AC02–06CH11357, DE-AC02-05CH11231, 06CH11357)
Topics
  • Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
  • Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Keywords
copper-binding proteins, copper homeostasis, skeletal muscle differentiation, myogenesis, myoblasts, MyoD, metallothionein, transcriptional regulation, copper accumulation, metalloproteomics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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