The sale will herald a year of unprecedented interest in the brief but dramatic life of the republican who was assassinated 73 years ago. Plans exist for three films of Collins' life, with the first, directed by Neil Jordan, who made the successful IRA drama The Crying Game, due to begin shooting later this year. Michael Cimino and Kevin Costner are also considering making movies about him.
The depiction of Collins' Requiem Mass by Sir John, one of the leading society painters of the time, is made all the more poignant because he and his wife Hazel were friends of Collins. Historians are divided over whether Hazel Lavery and Collins were lovers, or if it was just wishful thinking on her part. She had to be dissuaded from wearing widow's weeds at his funeral, as Collins was engaged to Kitty Kiernan when he died. Later Belfast-born Lavery's painting of his wife was used on Irish bank notes to symbolise Kathleen Ni Houlihan, Mother Ireland.
The international interest shown in the painting is a measure of the fascination with Collins. Some experts suggest it could match the previous record of £296,000 for a Lavery.
The film-makers planning movies of Collins' life will hardly need to embellish the plot: his career was tailor-made for an epic thriller. After his narrow escape from execution after the 1916 Easter Rising, Collins used the Irish Republican Brotherhood (a precursor of the IRA) to pioneer a closely-organised guerrilla movement, later emulated by independence movements all over the world.
During the final years of British rule Collins repeatedly eluded arrest, aided by tip-offs from his spies in the British headquarters at Dublin Castle. His personal grip on military activities, finance and intelligence held together a campaign that might otherwise have foundered. Playing on what the British least expected, he would chat with troops at checkpoints as he criss-crossed the city on two wheels, prompting comment that his was the first revolution conducted by bicycle.
He was also ruthless, ordering the assassination in a single morning of the "Cairo Gang" - 19 British agents closing in on his operations. Some were in bed with their wives when his gunmen, "The Twelve Apostles", came calling. This pre-emptive strike became the original Bloody Sunday, as British reprisals saw troops kill 14 and wound hundreds at a Gaelic football match in Dublin's Croke Park.
Collins recognised that in signing the Treaty with Britain, which created the Irish Free State and led to civil war, he had signed his own death warrant. His killing by former comrades on the anti-Treaty side traumatised the Irish nation. Even civil war prisoners opposing Collins wept and prayed for him when told of his death in an ambush in his home county of Cork.
Recent interest in Collins has led to reappraisals of his position in Irish history, identifying in his writings a vision of a dynamic, forward- looking country. Historian Joe Lee believes Collins was unique among independence leaders in pursuing "not only a new state but a new society". Anticipating a present-day "single Irish economy", Collins argued "a prosperous Ireland will mean a united Ireland".
Meanwhile, the other famous Collins attribute, his sex appeal, is unlikely to be passed over in Jordan's film. He has cast Liam Neeson, the six-foot actor known as "the Gael force", to play him.