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However, he avoided any admission of Church "guilt" over alleged complicity.
Since arriving in Israel as part of his Millennium Pilgrimage, the Pope has been under growing pressure to apologise for the Vatican's failure to speak out during the Holocaust.
The 79-year-old placed a prayer into the crevices of the Western (or Wailing) Wall, asking for God's forgiveness for "the behaviour of those who in the course of history have caused these children of yours to suffer".
"I assure the Jewish people the Catholic Church ... is deeply saddened by the hatred, acts of persecution and displays of anti-Semitism directed against the Jews by Christians at any time and in any place," the Pope said.
The pontiff added that there were "no words strong enough to deplore the terrible tragedy" of the Holocaust.
A spokesman for the pontiff said he had paused for a moment of private prayer - "something personal" - and laid a hand on the wall.
By placing his prayer, which was typewritten and signed by the Pope, in the wall he echoed the custom of Jewish worshippers over generations.
The prayer was taken from the wall by a government spokesman and placed in the archives of Yad Vashem, Israel's Holocaust memorial for the six million Jews killed by the Nazis.
Israeli cabinet minister Rabbi Michael Melchior, who hosted the Pope's visit, said he was "very moved" by the Pope's gesture.
The Pope is visiting the most sacred sites in Jerusalem at the climax of his week-long Millennium Pilgrimage to the Holy Land. He is the first pontiff to go there in 36 years.
John Paul II had repeatedly said he had dreamt of visiting the region since he was elected pontiff in 1978.
The visit to the holiest site of Islam, Christianity and Judaism, saw around 7,000 Israeli security forces deployed in the ancient city.
City police arrested several extreme right-wing Jewish residents amid fears of disturbances.
Earlier, the pontiff visited the Al Aqsa Mosque, the third-holiest Islamic shrine. He was greeted by the top Islamic cleric in Jerusalem and other Palestinian clerics and dignitaries.
Outside the mosque, more than a dozen Muslim protesters screamed at PLO officials after they met the pontiff.
The Pope's Millennium Pilgrimage was hailed as a great success.
A Vatican spokesman said: "The key to the success of this trip is that the Pope told everyone the truth without humiliating anybody. He spoke with love."
An Israeli official said: "The Middle East has already changed. Not so long ago it would have been unthinkable for the Pope to fly to Tel Aviv on Royal Jordanian Airlines and back to Rome on El Al."
During his trip, the Pope celebrated mass at the Church of the Holy Sepulchre, the site where Jesus is said to have been crucified and buried.
Following John Paul II's visit, Rabbi Michael Melchior announced that Israel would set up a forum to promote peace between Jews, Christians and Muslims.
The Pope travelled all over the world during his Papacy. In the latter years he suffered from Parkinson's disease and became increasingly frail but was determined to continue his overseas trips.
The Pope died at 2137 (1937 GMT) on Saturday 2 April 2005 after he failed to recover from a throat operation due to breathing problems.
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