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In September 2008, Dennings hoped to make Don De Lillo's novel End Zone into a film.Actors Sam Rockwell and Josh Hartnett were involved, but the project was not greenlit because of its controversial subject matter of nuclear war.
In 2002, Dennings appeared in the Disney Channel film The Scream Team as a teenager who stumbles into a group of ghosts.
She also starred in the teen romance Nick and Norah's Infinite Playlist, with Michael Cera.
Dennings played Norah Silverberg, the daughter of a famous record producer, and was nominated for the International Press Academy's Satellite Award for Best Actress for the performance.
Dennings starred in Charlie Bartlett in 2008, the story of a wealthy teenager (Anton Yelchin) who acts as a psychiatrist for his new public high school.
She played Susan Gardner, Bartlett's love interest, and the daughter of the school's principal (Robert Downey, Jr.).
From 2011 to 2017, she starred alongside Beth Behrs in the CBS sitcom 2 Broke Girls.
Dennings made her professional debut with an appearance on HBO's Sex and the City in 2000, in the episode "Hot Child in the City", playing an obnoxious 13-year-old who hires Samantha to handle publicity for her bat mitzvah.
Dennings and other rising stars were featured in the August 2009 issue of Vanity Fair, re-enacting scenes from famous Depression-era films, hers being Sydney Pollack's They Shoot Horses, Don't They? The following year, she starred in the independent feature Daydream Nation as a girl who moves from the city to a strange rural town, and is caught in a love triangle with her high school teacher (Josh Lucas) and a teenage drug dealer (Reece Thompson).
In May 2010, Dennings appeared in a music video for "40 Dogs (Like Romeo and Juliet)", a single by Austin, Texas-based musician Bob Schneider.
Beth Behrs co-stars as a Manhattan heiress who lost her inheritance, while Dennings plays a tough outspoken girl from Brooklyn.
Dennings starred in the drama film To Write Love on Her Arms (originally titled Renee) in 2012, with Chad Michael Murray and Rupert Friend.
She was cast for a five-episode run on The WB's Everwood, but the role was recast with Nora Zehetner.