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

Verdejo-Torres, Odette; Klein, David C.; Novoa-Aponte, Lorena; Carrazco-Carrillo, Jaime; Bonilla-Pinto, Denzel; Rivera, Antonio; Bakhshian, Arpie; Fitisemanu, Fa’alataitaua M.; Jiménez-González, Martha L.; Flinn, Lyra; Pezacki, Aidan T.; Lanzirotti, Antonio; Ortiz Frade, Luis Antonio; Chang, Christopher J.; Navea, Juan G.; Blaby-Haas, Crysten E.; Hainer, Sarah J.; Padilla-Benavides, Teresita

doi:10.1371/journal.pgen.1011495

Title: Cysteine Rich Intestinal Protein 2 is a copper-responsive regulator of skeletal muscle differentiation and metal homeostasis

Journal Article · 04 December 2024 · PLoS Genetics

DOI: https://doi.org/10.1371/journal.pgen.1011495 · OSTI ID:2497770

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Wesleyan University, Middletown, CT (United States)
Univ. of Pittsburgh, PA (United States); Progenra, Inc., Malvern, PA (United States)
Worcester Polytechnic Institute, MA (United States); National Institutes of Health (NIH), Bethesda, MD (United States)
Center of Research and Technologic Development in Electrochemistry (CIDETEQ) (Mexico)
Skidmore College, Saratoga Springs, NY (United States)
Princeton Univ., NJ (United States); University of California, Berkeley, CA (United States)
Univ. of Chicago, IL (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Molecular Foundry
Univ. of Pittsburgh, PA (United States)

Copper (Cu) is essential for respiration, neurotransmitter synthesis, oxidative stress response, and transcription regulation, with imbalances leading to neurological, cognitive, and muscular disorders. Here we show the role of a novel Cu-binding protein (Cu-BP) in mammalian transcriptional regulation, specifically on skeletal muscle differentiation using murine primary myoblasts. Utilizing synchrotron X-ray fluorescence-mass spectrometry, we identified murine cysteine-rich intestinal protein 2 (mCrip2) as a key Cu-BP abundant in both nuclear and cytosolic fractions. mCrip2 binds two to four Cu⁺ ions with high affinity and presents limited redox potential. CRISPR/Cas9-mediated deletion of mCrip2 impaired myogenesis, likely due to Cu accumulation in cells. CUT&RUN and transcriptome analyses revealed its association with gene promoters, including MyoD1 and metallothioneins, suggesting a novel Cu-responsive regulatory role for mCrip2. Our work describes the significance of mCrip2 in skeletal muscle differentiation and metal homeostasis, expanding understanding of the Cu-network in myoblasts. Copper (Cu) is essential for various cellular processes, including respiration and stress response, but imbalances can cause serious health issues. This study reveals a new Cu-binding protein (Cu-BP) involved in muscle development in primary myoblasts. Using unbiased metalloproteomic techniques and high throughput sequencing, we identified mCrip2 as a key Cu-BP found in cell nuclei and cytoplasm. mCrip2 binds up to four Cu⁺ ions and has a limited redox potential. Deleting mCrip2 using CRISPR/Cas9 disrupted muscle formation due to Cu accumulation. Further analyses showed that mCrip2 regulates the expression of genes like MyoD1, essential for muscle differentiation, and metallothioneins in response to copper supplementation. This research highlights the importance of mCrip2 in muscle development and metal homeostasis, providing new insights into the Cu-network in cells.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)

Grant/Contract Number:: AC02-05CH11231; AC02-06CH11357

OSTI ID:: 2497770

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 12 Vol. 20; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Title: Cysteine Rich Intestinal Protein 2 is a copper-responsive regulator of skeletal muscle differentiation and metal homeostasis

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