By Emily Stephenson and Mark Hosenball

WASHINGTON (Reuters) - The Clinton Foundation on multiple occasions during Hillary Clinton's tenure as secretary of state asked senior U.S. government officials to vet her husband's contacts with potentially controversial international figures, according to emails released by the State Department.

The emails, reviewed by Reuters, were part of a batch of nearly 400 messages recently released by the State Department after requests from the conservative group Citizens United, a group that has long been critical of the Clintons.

The exchanges show a top foreign policy adviser to the foundation sought guidance from the State Department on former President Bill Clinton's interactions with people including Syrian President Bashar al-Assad, Russian government officials and business leaders, and Gulnara Karimova, the socialite daughter of Uzbekistan’s late president.

The emails offer a glimpse of the intricate relationship between a private charity with a broad global mission and the State Department under the leadership of a secretary who is married to a former president.

Former government officials reached by Reuters said there was nothing inappropriate in the interactions of the foundation with the State Department over the potential meetings, some of which did not occur.

The latest batch of emails likely represents only a partial view of all the exchanges between the State Department and the foundation. It is unclear how frequently the foundation sought advice from the State Department on meetings involving Bill Clinton.

In one instance, the emails show Amitabh Desai, a foreign policy adviser to the foundation and to Bill Clinton, raised the possibility in 2009 of a meeting between Bill Clinton and Syrian President Assad. At the time, Assad wanted better ties with the West.

"Would this be concerning for State?" Desai wrote in an email alerting Hillary Clinton aide Jake Sullivan to the possible meeting.

"The Syrians expressed a keen interest in facilitating this," Desai said in an email a few days later.

The Syria visit was proposed to be tacked onto a forum Bill Clinton was invited to attend in Israel in November 2009, according to the emails. The meeting never happened, according to Martin Indyk, a former U.S. ambassador to Israel who helped to organize the trip.

The State Department sometimes communicates with charities, such as about circumstances that might involve the safety of Americans or highly sensitive diplomatic situations, but it typically does not vet their contacts with foreign leaders to this extent. State Department spokesman Elizabeth Trudeau said officials occasionally provide talking points and briefings to ex-presidents.

Much of Bill Clinton's communications with the State Department stemmed from an ethics agreement that was put in place when Hillary Clinton became secretary of state in 2009. The agreement was aimed at avoiding conflicts of interests stemming from contributions to the foundation and Bill Clinton’s paid speeches and consulting. Trudeau said these were "voluntary steps" taken to avoid "even the appearance of a conflict of interest."

Angel Urena, press secretary for Bill Clinton, said the requests for State Department input on potential meetings, talking points and other information “was done in order to inform the administration of President Clinton's interactions with foreign governments and dignitaries, so that the administration could in turn offer advice or voice any concerns." Urena said Bill Clinton had sought advice on his activities since he left office in 2001.

The Clinton Foundation referred questions to Urena. Hillary Clinton’s presidential campaign declined to comment.

CHARITY QUESTIONS LINGER

Clinton's campaign to win the Nov. 8 presidential election has been dogged by criticism of the Bill, Hillary & Chelsea Clinton Foundation, a global philanthropic organization.

The foundation has said it will stop accepting at least some foreign and corporate donations if Hillary Clinton becomes president and that Bill Clinton would resign from the foundation's board.

In one previously unreported email exchange, Desai wrote to the State Department in May 2012 informing officials that Bill Clinton would travel to Monaco to raise money for the foundation at an event where he might cross paths with the elder daughter of the Uzbekistan president.

Gulnara Karimova, a businesswoman and pop star, was described in a 2005 cable from a U.S. embassy official as the "single most hated person in Uzbekistan" because of her flamboyant lifestyle in an authoritarian country. She has since come under investigation in an international bribery scandal.

Ahead of the event in Monaco, Desai wrote that the organizers had invited Karimova to be one of the event’s sponsors "apparently without our approval."

The Uzbekistan president's daughter "will be listed in the program and will see (Bill Clinton)," he said. "Would (the U.S. government) have concerns? If so, we can go back to organizer and ask them to return her sponsorship and disinvite her, however I assume that would ruffle some feathers,” Desai said.

The emails released to Citizens United don't contain a reply to Desai's inquiry. However, a collection of photos from the Monaco event posted on the internet show Karimova attended it. They do not show any pictures of her with Bill Clinton.

(Editing by Caren Bohan and Edward Tobin)