TY - JOUR
T1 - Placental senescence pathophysiology is shared between peripartum cardiomyopathy and preeclampsia in mouse and human
AU - IPAC Investigators
AU - Roh, Jason D
AU - Castro, Claire
AU - Yu, Andy
AU - Rana, Sarosh
AU - Shahul, Sajid
AU - Gray, Kathryn J
AU - Honigberg, Michael C
AU - Ricke-Hoch, Melanie
AU - Iwamoto, Yoshiko
AU - Yeri, Ashish
AU - Kitchen, Robert
AU - Guerra, Justin Baldovino
AU - Hobson, Ryan
AU - Chaudhari, Vinita
AU - Chang, Bliss
AU - Sarma, Amy
AU - Lerchenmüller, Carolin
AU - Al Sayed, Zeina R
AU - Diaz Verdugo, Carmen
AU - Xia, Peng
AU - Skarbianskis, Niv
AU - Zeisel, Amit
AU - Bauersachs, Johann
AU - Kirkland, James L
AU - Karumanchi, S Ananth
AU - Gorcsan, John
AU - Sugahara, Masataka
AU - Damp, Julie
AU - Hanley-Yanez, Karen
AU - Ellinor, Patrick T
AU - Arany, Zoltan
AU - McNamara, Dennis M
AU - Hilfiker-Kleiner, Denise
AU - Rosenzweig, Anthony
PY - 2024/4/17
Y1 - 2024/4/17
N2 - Peripartum cardiomyopathy (PPCM) is an idiopathic form of pregnancy-induced heart failure associated with preeclampsia. Circulating factors in late pregnancy are thought to contribute to both diseases, suggesting a common underlying pathophysiological process. However, what drives this process remains unclear. Using serum proteomics, we identified the senescence-associated secretory phenotype (SASP), a marker of cellular senescence associated with biological aging, as the most highly up-regulated pathway in young women with PPCM or preeclampsia. Placentas from women with preeclampsia displayed multiple markers of amplified senescence and tissue aging, as well as overall increased gene expression of 28 circulating proteins that contributed to SASP pathway enrichment in serum samples from patients with preeclampsia or PPCM. The most highly expressed placental SASP factor, activin A, was associated with cardiac dysfunction or heart failure severity in women with preeclampsia or PPCM. In a murine model of PPCM induced by cardiomyocyte-specific deletion of the gene encoding peroxisome proliferator-activated receptor γ coactivator-1α, inhibiting activin A signaling in the early postpartum period with a monoclonal antibody to the activin type II receptor improved heart function. In addition, attenuating placental senescence with the senolytic compound fisetin in late pregnancy improved cardiac function in these animals. These findings link senescence biology to cardiac dysfunction in pregnancy and help to elucidate the pathogenesis underlying cardiovascular diseases of pregnancy.
AB - Peripartum cardiomyopathy (PPCM) is an idiopathic form of pregnancy-induced heart failure associated with preeclampsia. Circulating factors in late pregnancy are thought to contribute to both diseases, suggesting a common underlying pathophysiological process. However, what drives this process remains unclear. Using serum proteomics, we identified the senescence-associated secretory phenotype (SASP), a marker of cellular senescence associated with biological aging, as the most highly up-regulated pathway in young women with PPCM or preeclampsia. Placentas from women with preeclampsia displayed multiple markers of amplified senescence and tissue aging, as well as overall increased gene expression of 28 circulating proteins that contributed to SASP pathway enrichment in serum samples from patients with preeclampsia or PPCM. The most highly expressed placental SASP factor, activin A, was associated with cardiac dysfunction or heart failure severity in women with preeclampsia or PPCM. In a murine model of PPCM induced by cardiomyocyte-specific deletion of the gene encoding peroxisome proliferator-activated receptor γ coactivator-1α, inhibiting activin A signaling in the early postpartum period with a monoclonal antibody to the activin type II receptor improved heart function. In addition, attenuating placental senescence with the senolytic compound fisetin in late pregnancy improved cardiac function in these animals. These findings link senescence biology to cardiac dysfunction in pregnancy and help to elucidate the pathogenesis underlying cardiovascular diseases of pregnancy.
KW - Humans
KW - Pregnancy
KW - Female
KW - Mice
KW - Animals
KW - Pre-Eclampsia
KW - Peripartum Period
KW - Placenta
KW - Cardiomyopathies
KW - Heart Failure
KW - Transcription Factors
KW - Heart Diseases
U2 - 10.1126/scitranslmed.adi0077
DO - 10.1126/scitranslmed.adi0077
M3 - Article
C2 - 38630848
SN - 1946-6234
VL - 16
SP - eadi0077
JO - Science translational medicine
JF - Science translational medicine
IS - 743
ER -