Dataset Information

CALCIUM-DEPENDENT PROTEOLYSIS OF THE ARABIDOPSIS DAMP PRECURSOR PROPEP1 BY THE CYSTEINE PROTEASE METACASPASE4 REVEALS A CONSERVED MECHANISM FOR IMMEDIATE RELEASE OF PEPTIDE SIGNALS DURING WOUND RESPONSES

ABSTRACT: In animals, one of the most immediate responses to tissue wounding comprises the release of peptide signals such as interleukins from their precursor proteins. Although the wound response has been intensively studied in plants as well, little is known about plant peptides with cytokine-like functions. Here we report that in Arabidopsis thaliana, wounding triggers the instantaneous activation of the METACASPASE4 cysteine protease and subsequent cleavage of the PROPEP1 precursor to release the mature peptide signal PEP1, which induces basal immunity against pathogens. Furthermore, confocal microscopy of targeted cell damage by laser wounding revealed that the inactive zymogen of MC4 and PROPEP1 reside in the cytosol until a constitutive increase in calcium concentration upon cell membrane integrity loss triggers MC4 activation and PROPEP1 cleavage. PROPEP1 cleavage and PEP1 release is restricted to only a few cells surrounding the damaged site. Our results highlight the similarities of the spatiotemporal dynamics and control mechanisms of the plant wound response as an example for convergent evolution with respect to the mammalian system, in which calpain releases IL1-α from its precursor.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Arabidopsis Thaliana (mouse-ear Cress)

TISSUE(S): Root

SUBMITTER: An Staes

LAB HEAD: Kris Gevaert

PROVIDER: PXD005740 | Pride | 2019-04-23

REPOSITORIES: Pride

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Publications

Damage on plants activates Ca2+-dependent metacaspases for release of immunomodulatory peptides.

Hander Tim T Fernández-Fernández Álvaro D ÁD Kumpf Robert P RP Willems Patrick P Schatowitz Hendrik H Rombaut Debbie D Staes An A Nolf Jonah J Pottie Robin R Yao Panfeng P Gonçalves Amanda A Pavie Benjamin B Boller Thomas T Gevaert Kris K Van Breusegem Frank F Bartels Sebastian S Stael Simon S

Science (New York, N.Y.) 20190301 6433

Physical damage to cells leads to the release of immunomodulatory peptides to elicit a wound defense response in the surrounding tissue. In Arabidopsis thaliana, the plant elicitor peptide 1 (Pep1) is processed from its protein precursor, PRECURSOR OF PEP1 (PROPEP1). We demonstrate that upon damage, both at the tissue and single-cell levels, the cysteine protease METACASPASE4 (MC4) is instantly and spatiotemporally activated by binding high levels of Ca2+ and is necessary and s ...[more]

PMID: 30898901

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Project description:Wound healing is a complex process regulated by various cell types and a plethora of mediators. While interactions between wounded skin and the hair follicles (HFs) could induce HF neogenesis or promote wound healing, it remains unknown whether the wound healing-associated signaling milieu can be manipulated to protect against alopecia, such as chemotherapy-induced alopecia (CIA). Utilizing a well-established neonatal rat model of CIA, we show here that skin wounding protects from alopecia caused by several clinically relevant chemotherapeutic regimens, and that protection is dependent on the time of wounding and hair cycle stage. Gene expression profiling unveiled a significant increase in interleukin-1 beta (IL-1β) mediated signaling by skin wounding. Subsequently, we showed that IL-1β is sufficient and indispensable for mediating the CIA-protective effect. Administration of IL-1β alone to unwounded rats exhibited local CIA protection while IL-1β neutralization abrogated CIA protection by wounding. Mechanistically, IL-1β retarded postnatal HF morphogenesis, making HFs at the wound sites or IL-1β treated areas damage-resistant while the rats developed total alopecia elsewhere. We conclude that wound healing switches the cutaneous cytokine milieu to an IL-1β-dominated state thus retarding HF growth progression and rendering the HFs resistant to chemotherapy agents. In the future, manipulation of HF progression through interfering with the IL-1β signaling milieu may provide therapeutic benefits to a variety of conditions, from prevention of CIA to inhibition of hair growth and treatment of hirsutism. In this experiment, we used the Rat MI-Ready array comprised of over 34,000 transcript probes for gene and alternative splice products in ENSEMBL release 37 to profile gene expression changes during acute wound healing in rat skin. 16,198 Selected rat probes were above threshold in at least one group. 3,239 significant genes were found (FDR < 0.1).

Dataset Information

CALCIUM-DEPENDENT PROTEOLYSIS OF THE ARABIDOPSIS DAMP PRECURSOR PROPEP1 BY THE CYSTEINE PROTEASE METACASPASE4 REVEALS A CONSERVED MECHANISM FOR IMMEDIATE RELEASE OF PEPTIDE SIGNALS DURING WOUND RESPONSES

Publications

Damage on plants activates Ca<sup>2+</sup>-dependent metacaspases for release of immunomodulatory peptides.

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